diff --git a/assets/prompts/assistant_system_prompt.hbs b/assets/prompts/assistant_system_prompt.hbs
index eb91c4f4a8..1aca0a938b 100644
--- a/assets/prompts/assistant_system_prompt.hbs
+++ b/assets/prompts/assistant_system_prompt.hbs
@@ -73,9 +73,9 @@ There are project rules that apply to these root directories:
 {{/each}}
 {{/if}}
 
-{{#if has_default_user_rules}}
+{{#if has_user_rules}}
 The user has specified the following rules that should be applied:
-{{#each default_user_rules}}
+{{#each user_rules}}
 
 {{#if title}}
 Rules title: {{title}}
diff --git a/crates/agent/src/active_thread.rs b/crates/agent/src/active_thread.rs
index 2a4a00cf23..a0dd54218d 100644
--- a/crates/agent/src/active_thread.rs
+++ b/crates/agent/src/active_thread.rs
@@ -1,4 +1,4 @@
-use crate::context::{AssistantContext, ContextId, format_context_as_string};
+use crate::context::{AssistantContext, ContextId, RULES_ICON, format_context_as_string};
 use crate::context_picker::MentionLink;
 use crate::thread::{
     LastRestoreCheckpoint, MessageId, MessageSegment, Thread, ThreadError, ThreadEvent,
@@ -688,6 +688,12 @@ fn open_markdown_link(
             }
         }),
         Some(MentionLink::Fetch(url)) => cx.open_url(&url),
+        Some(MentionLink::Rules(prompt_id)) => window.dispatch_action(
+            Box::new(OpenPromptLibrary {
+                prompt_to_select: Some(prompt_id.0),
+            }),
+            cx,
+        ),
         None => cx.open_url(&text),
     }
 }
@@ -2957,10 +2963,10 @@ impl ActiveThread {
             return div().into_any();
         };
 
-        let default_user_rules_text = if project_context.default_user_rules.is_empty() {
+        let user_rules_text = if project_context.user_rules.is_empty() {
             None
-        } else if project_context.default_user_rules.len() == 1 {
-            let user_rules = &project_context.default_user_rules[0];
+        } else if project_context.user_rules.len() == 1 {
+            let user_rules = &project_context.user_rules[0];
 
             match user_rules.title.as_ref() {
                 Some(title) => Some(format!("Using \"{title}\" user rule")),
@@ -2969,14 +2975,14 @@ impl ActiveThread {
         } else {
             Some(format!(
                 "Using {} user rules",
-                project_context.default_user_rules.len()
+                project_context.user_rules.len()
             ))
         };
 
-        let first_default_user_rules_id = project_context
-            .default_user_rules
+        let first_user_rules_id = project_context
+            .user_rules
             .first()
-            .map(|user_rules| user_rules.uuid);
+            .map(|user_rules| user_rules.uuid.0);
 
         let rules_files = project_context
             .worktrees
@@ -2993,7 +2999,7 @@ impl ActiveThread {
             rules_files => Some(format!("Using {} project rules files", rules_files.len())),
         };
 
-        if default_user_rules_text.is_none() && rules_file_text.is_none() {
+        if user_rules_text.is_none() && rules_file_text.is_none() {
             return div().into_any();
         }
 
@@ -3001,45 +3007,42 @@ impl ActiveThread {
             .pt_2()
             .px_2p5()
             .gap_1()
-            .when_some(
-                default_user_rules_text,
-                |parent, default_user_rules_text| {
-                    parent.child(
-                        h_flex()
-                            .w_full()
-                            .child(
-                                Icon::new(IconName::File)
-                                    .size(IconSize::XSmall)
-                                    .color(Color::Disabled),
-                            )
-                            .child(
-                                Label::new(default_user_rules_text)
-                                    .size(LabelSize::XSmall)
-                                    .color(Color::Muted)
-                                    .truncate()
-                                    .buffer_font(cx)
-                                    .ml_1p5()
-                                    .mr_0p5(),
-                            )
-                            .child(
-                                IconButton::new("open-prompt-library", IconName::ArrowUpRightAlt)
-                                    .shape(ui::IconButtonShape::Square)
-                                    .icon_size(IconSize::XSmall)
-                                    .icon_color(Color::Ignored)
-                                    // TODO: Figure out a way to pass focus handle here so we can display the `OpenPromptLibrary`  keybinding
-                                    .tooltip(Tooltip::text("View User Rules"))
-                                    .on_click(move |_event, window, cx| {
-                                        window.dispatch_action(
-                                            Box::new(OpenPromptLibrary {
-                                                prompt_to_focus: first_default_user_rules_id,
-                                            }),
-                                            cx,
-                                        )
-                                    }),
-                            ),
-                    )
-                },
-            )
+            .when_some(user_rules_text, |parent, user_rules_text| {
+                parent.child(
+                    h_flex()
+                        .w_full()
+                        .child(
+                            Icon::new(RULES_ICON)
+                                .size(IconSize::XSmall)
+                                .color(Color::Disabled),
+                        )
+                        .child(
+                            Label::new(user_rules_text)
+                                .size(LabelSize::XSmall)
+                                .color(Color::Muted)
+                                .truncate()
+                                .buffer_font(cx)
+                                .ml_1p5()
+                                .mr_0p5(),
+                        )
+                        .child(
+                            IconButton::new("open-prompt-library", IconName::ArrowUpRightAlt)
+                                .shape(ui::IconButtonShape::Square)
+                                .icon_size(IconSize::XSmall)
+                                .icon_color(Color::Ignored)
+                                // TODO: Figure out a way to pass focus handle here so we can display the `OpenPromptLibrary`  keybinding
+                                .tooltip(Tooltip::text("View User Rules"))
+                                .on_click(move |_event, window, cx| {
+                                    window.dispatch_action(
+                                        Box::new(OpenPromptLibrary {
+                                            prompt_to_select: first_user_rules_id,
+                                        }),
+                                        cx,
+                                    )
+                                }),
+                        ),
+                )
+            })
             .when_some(rules_file_text, |parent, rules_file_text| {
                 parent.child(
                     h_flex()
@@ -3316,6 +3319,12 @@ pub(crate) fn open_context(
                 }
             })
         }
+        AssistantContext::Rules(rules_context) => window.dispatch_action(
+            Box::new(OpenPromptLibrary {
+                prompt_to_select: Some(rules_context.prompt_id.0),
+            }),
+            cx,
+        ),
     }
 }
 
diff --git a/crates/agent/src/assistant_panel.rs b/crates/agent/src/assistant_panel.rs
index cea3a781a2..82c7b2be9d 100644
--- a/crates/agent/src/assistant_panel.rs
+++ b/crates/agent/src/assistant_panel.rs
@@ -25,7 +25,7 @@ use language_model::{LanguageModelProviderTosView, LanguageModelRegistry};
 use language_model_selector::ToggleModelSelector;
 use project::Project;
 use prompt_library::{PromptLibrary, open_prompt_library};
-use prompt_store::{PromptBuilder, PromptId};
+use prompt_store::{PromptBuilder, PromptId, UserPromptId};
 use proto::Plan;
 use settings::{Settings, update_settings_file};
 use time::UtcOffset;
@@ -79,11 +79,11 @@ pub fn init(cx: &mut App) {
                         panel.update(cx, |panel, cx| panel.new_prompt_editor(window, cx));
                     }
                 })
-                .register_action(|workspace, _: &OpenPromptLibrary, window, cx| {
+                .register_action(|workspace, action: &OpenPromptLibrary, window, cx| {
                     if let Some(panel) = workspace.panel::<AssistantPanel>(cx) {
                         workspace.focus_panel::<AssistantPanel>(window, cx);
                         panel.update(cx, |panel, cx| {
-                            panel.deploy_prompt_library(&OpenPromptLibrary::default(), window, cx)
+                            panel.deploy_prompt_library(action, window, cx)
                         });
                     }
                 })
@@ -502,7 +502,9 @@ impl AssistantPanel {
                     None,
                 ))
             }),
-            action.prompt_to_focus.map(|uuid| PromptId::User { uuid }),
+            action.prompt_to_select.map(|uuid| PromptId::User {
+                uuid: UserPromptId(uuid),
+            }),
             cx,
         )
         .detach_and_log_err(cx);
diff --git a/crates/agent/src/context.rs b/crates/agent/src/context.rs
index 0770c5b4d7..b6213cde54 100644
--- a/crates/agent/src/context.rs
+++ b/crates/agent/src/context.rs
@@ -4,6 +4,7 @@ use gpui::{App, Entity, SharedString};
 use language::{Buffer, File};
 use language_model::LanguageModelRequestMessage;
 use project::{ProjectPath, Worktree};
+use prompt_store::UserPromptId;
 use rope::Point;
 use serde::{Deserialize, Serialize};
 use text::{Anchor, BufferId};
@@ -12,6 +13,8 @@ use util::post_inc;
 
 use crate::thread::Thread;
 
+pub const RULES_ICON: IconName = IconName::Context;
+
 #[derive(Debug, PartialEq, Eq, PartialOrd, Ord, Hash, Clone, Copy, Serialize, Deserialize)]
 pub struct ContextId(pub(crate) usize);
 
@@ -20,6 +23,7 @@ impl ContextId {
         Self(post_inc(&mut self.0))
     }
 }
+
 pub enum ContextKind {
     File,
     Directory,
@@ -27,6 +31,7 @@ pub enum ContextKind {
     Excerpt,
     FetchedUrl,
     Thread,
+    Rules,
 }
 
 impl ContextKind {
@@ -38,6 +43,7 @@ impl ContextKind {
             ContextKind::Excerpt => IconName::Code,
             ContextKind::FetchedUrl => IconName::Globe,
             ContextKind::Thread => IconName::MessageBubbles,
+            ContextKind::Rules => RULES_ICON,
         }
     }
 }
@@ -50,6 +56,7 @@ pub enum AssistantContext {
     FetchedUrl(FetchedUrlContext),
     Thread(ThreadContext),
     Excerpt(ExcerptContext),
+    Rules(RulesContext),
 }
 
 impl AssistantContext {
@@ -61,6 +68,7 @@ impl AssistantContext {
             Self::FetchedUrl(url) => url.id,
             Self::Thread(thread) => thread.id,
             Self::Excerpt(excerpt) => excerpt.id,
+            Self::Rules(rules) => rules.id,
         }
     }
 }
@@ -168,6 +176,14 @@ pub struct ExcerptContext {
     pub context_buffer: ContextBuffer,
 }
 
+#[derive(Debug, Clone)]
+pub struct RulesContext {
+    pub id: ContextId,
+    pub prompt_id: UserPromptId,
+    pub title: SharedString,
+    pub text: SharedString,
+}
+
 /// Formats a collection of contexts into a string representation
 pub fn format_context_as_string<'a>(
     contexts: impl Iterator<Item = &'a AssistantContext>,
@@ -179,6 +195,7 @@ pub fn format_context_as_string<'a>(
     let mut excerpt_context = Vec::new();
     let mut fetch_context = Vec::new();
     let mut thread_context = Vec::new();
+    let mut rules_context = Vec::new();
 
     for context in contexts {
         match context {
@@ -188,6 +205,7 @@ pub fn format_context_as_string<'a>(
             AssistantContext::Excerpt(context) => excerpt_context.push(context),
             AssistantContext::FetchedUrl(context) => fetch_context.push(context),
             AssistantContext::Thread(context) => thread_context.push(context),
+            AssistantContext::Rules(context) => rules_context.push(context),
         }
     }
 
@@ -197,6 +215,7 @@ pub fn format_context_as_string<'a>(
         && excerpt_context.is_empty()
         && fetch_context.is_empty()
         && thread_context.is_empty()
+        && rules_context.is_empty()
     {
         return None;
     }
@@ -263,6 +282,18 @@ pub fn format_context_as_string<'a>(
         result.push_str("</conversation_threads>\n");
     }
 
+    if !rules_context.is_empty() {
+        result.push_str(
+            "<user_rules>\n\
+            The user has specified the following rules that should be applied:\n\n",
+        );
+        for context in &rules_context {
+            result.push_str(&context.text);
+            result.push('\n');
+        }
+        result.push_str("</user_rules>\n");
+    }
+
     result.push_str("</context>\n");
     Some(result)
 }
diff --git a/crates/agent/src/context_picker.rs b/crates/agent/src/context_picker.rs
index 9e578c4fc0..ce08179fb9 100644
--- a/crates/agent/src/context_picker.rs
+++ b/crates/agent/src/context_picker.rs
@@ -1,6 +1,7 @@
 mod completion_provider;
 mod fetch_context_picker;
 mod file_context_picker;
+mod rules_context_picker;
 mod symbol_context_picker;
 mod thread_context_picker;
 
@@ -18,17 +19,22 @@ use gpui::{
 };
 use multi_buffer::MultiBufferRow;
 use project::{Entry, ProjectPath};
+use prompt_store::UserPromptId;
+use rules_context_picker::RulesContextEntry;
 use symbol_context_picker::SymbolContextPicker;
 use thread_context_picker::{ThreadContextEntry, render_thread_context_entry};
 use ui::{
     ButtonLike, ContextMenu, ContextMenuEntry, ContextMenuItem, Disclosure, TintColor, prelude::*,
 };
+use uuid::Uuid;
 use workspace::{Workspace, notifications::NotifyResultExt};
 
 use crate::AssistantPanel;
+use crate::context::RULES_ICON;
 pub use crate::context_picker::completion_provider::ContextPickerCompletionProvider;
 use crate::context_picker::fetch_context_picker::FetchContextPicker;
 use crate::context_picker::file_context_picker::FileContextPicker;
+use crate::context_picker::rules_context_picker::RulesContextPicker;
 use crate::context_picker::thread_context_picker::ThreadContextPicker;
 use crate::context_store::ContextStore;
 use crate::thread::ThreadId;
@@ -40,6 +46,7 @@ enum ContextPickerMode {
     Symbol,
     Fetch,
     Thread,
+    Rules,
 }
 
 impl TryFrom<&str> for ContextPickerMode {
@@ -51,6 +58,7 @@ impl TryFrom<&str> for ContextPickerMode {
             "symbol" => Ok(Self::Symbol),
             "fetch" => Ok(Self::Fetch),
             "thread" => Ok(Self::Thread),
+            "rules" => Ok(Self::Rules),
             _ => Err(format!("Invalid context picker mode: {}", value)),
         }
     }
@@ -63,6 +71,7 @@ impl ContextPickerMode {
             Self::Symbol => "symbol",
             Self::Fetch => "fetch",
             Self::Thread => "thread",
+            Self::Rules => "rules",
         }
     }
 
@@ -72,6 +81,7 @@ impl ContextPickerMode {
             Self::Symbol => "Symbols",
             Self::Fetch => "Fetch",
             Self::Thread => "Threads",
+            Self::Rules => "Rules",
         }
     }
 
@@ -81,6 +91,7 @@ impl ContextPickerMode {
             Self::Symbol => IconName::Code,
             Self::Fetch => IconName::Globe,
             Self::Thread => IconName::MessageBubbles,
+            Self::Rules => RULES_ICON,
         }
     }
 }
@@ -92,6 +103,7 @@ enum ContextPickerState {
     Symbol(Entity<SymbolContextPicker>),
     Fetch(Entity<FetchContextPicker>),
     Thread(Entity<ThreadContextPicker>),
+    Rules(Entity<RulesContextPicker>),
 }
 
 pub(super) struct ContextPicker {
@@ -253,6 +265,19 @@ impl ContextPicker {
                     }));
                 }
             }
+            ContextPickerMode::Rules => {
+                if let Some(thread_store) = self.thread_store.as_ref() {
+                    self.mode = ContextPickerState::Rules(cx.new(|cx| {
+                        RulesContextPicker::new(
+                            thread_store.clone(),
+                            context_picker.clone(),
+                            self.context_store.clone(),
+                            window,
+                            cx,
+                        )
+                    }));
+                }
+            }
         }
 
         cx.notify();
@@ -381,6 +406,7 @@ impl ContextPicker {
             ContextPickerState::Symbol(entity) => entity.update(cx, |_, cx| cx.notify()),
             ContextPickerState::Fetch(entity) => entity.update(cx, |_, cx| cx.notify()),
             ContextPickerState::Thread(entity) => entity.update(cx, |_, cx| cx.notify()),
+            ContextPickerState::Rules(entity) => entity.update(cx, |_, cx| cx.notify()),
         }
     }
 }
@@ -395,6 +421,7 @@ impl Focusable for ContextPicker {
             ContextPickerState::Symbol(symbol_picker) => symbol_picker.focus_handle(cx),
             ContextPickerState::Fetch(fetch_picker) => fetch_picker.focus_handle(cx),
             ContextPickerState::Thread(thread_picker) => thread_picker.focus_handle(cx),
+            ContextPickerState::Rules(user_rules_picker) => user_rules_picker.focus_handle(cx),
         }
     }
 }
@@ -410,6 +437,9 @@ impl Render for ContextPicker {
                 ContextPickerState::Symbol(symbol_picker) => parent.child(symbol_picker.clone()),
                 ContextPickerState::Fetch(fetch_picker) => parent.child(fetch_picker.clone()),
                 ContextPickerState::Thread(thread_picker) => parent.child(thread_picker.clone()),
+                ContextPickerState::Rules(user_rules_picker) => {
+                    parent.child(user_rules_picker.clone())
+                }
             })
     }
 }
@@ -431,6 +461,7 @@ fn supported_context_picker_modes(
     ];
     if thread_store.is_some() {
         modes.push(ContextPickerMode::Thread);
+        modes.push(ContextPickerMode::Rules);
     }
     modes
 }
@@ -626,6 +657,7 @@ pub enum MentionLink {
     Symbol(ProjectPath, String),
     Fetch(String),
     Thread(ThreadId),
+    Rules(UserPromptId),
 }
 
 impl MentionLink {
@@ -633,14 +665,16 @@ impl MentionLink {
     const SYMBOL: &str = "@symbol";
     const THREAD: &str = "@thread";
     const FETCH: &str = "@fetch";
+    const RULES: &str = "@rules";
 
     const SEPARATOR: &str = ":";
 
     pub fn is_valid(url: &str) -> bool {
         url.starts_with(Self::FILE)
             || url.starts_with(Self::SYMBOL)
-            || url.starts_with(Self::FETCH)
             || url.starts_with(Self::THREAD)
+            || url.starts_with(Self::FETCH)
+            || url.starts_with(Self::RULES)
     }
 
     pub fn for_file(file_name: &str, full_path: &str) -> String {
@@ -657,12 +691,16 @@ impl MentionLink {
         )
     }
 
+    pub fn for_thread(thread: &ThreadContextEntry) -> String {
+        format!("[@{}]({}:{})", thread.summary, Self::THREAD, thread.id)
+    }
+
     pub fn for_fetch(url: &str) -> String {
         format!("[@{}]({}:{})", url, Self::FETCH, url)
     }
 
-    pub fn for_thread(thread: &ThreadContextEntry) -> String {
-        format!("[@{}]({}:{})", thread.summary, Self::THREAD, thread.id)
+    pub fn for_rules(rules: &RulesContextEntry) -> String {
+        format!("[@{}]({}:{})", rules.title, Self::RULES, rules.prompt_id.0)
     }
 
     pub fn try_parse(link: &str, workspace: &Entity<Workspace>, cx: &App) -> Option<Self> {
@@ -706,6 +744,10 @@ impl MentionLink {
                 Some(MentionLink::Thread(thread_id))
             }
             Self::FETCH => Some(MentionLink::Fetch(argument.to_string())),
+            Self::RULES => {
+                let prompt_id = UserPromptId(Uuid::try_parse(argument).ok()?);
+                Some(MentionLink::Rules(prompt_id))
+            }
             _ => None,
         }
     }
diff --git a/crates/agent/src/context_picker/completion_provider.rs b/crates/agent/src/context_picker/completion_provider.rs
index efa1cf5431..6703e93d66 100644
--- a/crates/agent/src/context_picker/completion_provider.rs
+++ b/crates/agent/src/context_picker/completion_provider.rs
@@ -14,11 +14,13 @@ use http_client::HttpClientWithUrl;
 use language::{Buffer, CodeLabel, HighlightId};
 use lsp::CompletionContext;
 use project::{Completion, CompletionIntent, ProjectPath, Symbol, WorktreeId};
+use prompt_store::PromptId;
 use rope::Point;
 use text::{Anchor, ToPoint};
 use ui::prelude::*;
 use workspace::Workspace;
 
+use crate::context::RULES_ICON;
 use crate::context_picker::file_context_picker::search_files;
 use crate::context_picker::symbol_context_picker::search_symbols;
 use crate::context_store::ContextStore;
@@ -26,6 +28,7 @@ use crate::thread_store::ThreadStore;
 
 use super::fetch_context_picker::fetch_url_content;
 use super::file_context_picker::FileMatch;
+use super::rules_context_picker::{RulesContextEntry, search_rules};
 use super::symbol_context_picker::SymbolMatch;
 use super::thread_context_picker::{ThreadContextEntry, ThreadMatch, search_threads};
 use super::{
@@ -38,6 +41,7 @@ pub(crate) enum Match {
     File(FileMatch),
     Thread(ThreadMatch),
     Fetch(SharedString),
+    Rules(RulesContextEntry),
     Mode(ModeMatch),
 }
 
@@ -54,6 +58,7 @@ impl Match {
             Match::Thread(_) => 1.,
             Match::Symbol(_) => 1.,
             Match::Fetch(_) => 1.,
+            Match::Rules(_) => 1.,
         }
     }
 }
@@ -112,6 +117,21 @@ fn search(
                 Task::ready(Vec::new())
             }
         }
+        Some(ContextPickerMode::Rules) => {
+            if let Some(thread_store) = thread_store.as_ref().and_then(|t| t.upgrade()) {
+                let search_rules_task =
+                    search_rules(query.clone(), cancellation_flag.clone(), thread_store, cx);
+                cx.background_spawn(async move {
+                    search_rules_task
+                        .await
+                        .into_iter()
+                        .map(Match::Rules)
+                        .collect::<Vec<_>>()
+                })
+            } else {
+                Task::ready(Vec::new())
+            }
+        }
         None => {
             if query.is_empty() {
                 let mut matches = recent_entries
@@ -287,6 +307,60 @@ impl ContextPickerCompletionProvider {
         }
     }
 
+    fn completion_for_rules(
+        rules: RulesContextEntry,
+        excerpt_id: ExcerptId,
+        source_range: Range<Anchor>,
+        editor: Entity<Editor>,
+        context_store: Entity<ContextStore>,
+        thread_store: Entity<ThreadStore>,
+    ) -> Completion {
+        let new_text = MentionLink::for_rules(&rules);
+        let new_text_len = new_text.len();
+        Completion {
+            replace_range: source_range.clone(),
+            new_text,
+            label: CodeLabel::plain(rules.title.to_string(), None),
+            documentation: None,
+            insert_text_mode: None,
+            source: project::CompletionSource::Custom,
+            icon_path: Some(RULES_ICON.path().into()),
+            confirm: Some(confirm_completion_callback(
+                RULES_ICON.path().into(),
+                rules.title.clone(),
+                excerpt_id,
+                source_range.start,
+                new_text_len,
+                editor.clone(),
+                move |cx| {
+                    let prompt_uuid = rules.prompt_id;
+                    let prompt_id = PromptId::User { uuid: prompt_uuid };
+                    let context_store = context_store.clone();
+                    let Some(prompt_store) = thread_store.read(cx).prompt_store() else {
+                        log::error!("Can't add user rules as prompt store is missing.");
+                        return;
+                    };
+                    let prompt_store = prompt_store.read(cx);
+                    let Some(metadata) = prompt_store.metadata(prompt_id) else {
+                        return;
+                    };
+                    let Some(title) = metadata.title else {
+                        return;
+                    };
+                    let text_task = prompt_store.load(prompt_id, cx);
+
+                    cx.spawn(async move |cx| {
+                        let text = text_task.await?;
+                        context_store.update(cx, |context_store, cx| {
+                            context_store.add_rules(prompt_uuid, title, text, false, cx)
+                        })
+                    })
+                    .detach_and_log_err(cx);
+                },
+            )),
+        }
+    }
+
     fn completion_for_fetch(
         source_range: Range<Anchor>,
         url_to_fetch: SharedString,
@@ -593,6 +667,17 @@ impl CompletionProvider for ContextPickerCompletionProvider {
                                 thread_store,
                             ))
                         }
+                        Match::Rules(user_rules) => {
+                            let thread_store = thread_store.as_ref().and_then(|t| t.upgrade())?;
+                            Some(Self::completion_for_rules(
+                                user_rules,
+                                excerpt_id,
+                                source_range.clone(),
+                                editor.clone(),
+                                context_store.clone(),
+                                thread_store,
+                            ))
+                        }
                         Match::Fetch(url) => Some(Self::completion_for_fetch(
                             source_range.clone(),
                             url,
diff --git a/crates/agent/src/context_picker/rules_context_picker.rs b/crates/agent/src/context_picker/rules_context_picker.rs
new file mode 100644
index 0000000000..4c1fc65303
--- /dev/null
+++ b/crates/agent/src/context_picker/rules_context_picker.rs
@@ -0,0 +1,248 @@
+use std::sync::Arc;
+use std::sync::atomic::AtomicBool;
+
+use anyhow::anyhow;
+use gpui::{App, DismissEvent, Entity, FocusHandle, Focusable, Task, WeakEntity};
+use picker::{Picker, PickerDelegate};
+use prompt_store::{PromptId, UserPromptId};
+use ui::{ListItem, prelude::*};
+
+use crate::context::RULES_ICON;
+use crate::context_picker::ContextPicker;
+use crate::context_store::{self, ContextStore};
+use crate::thread_store::ThreadStore;
+
+pub struct RulesContextPicker {
+    picker: Entity<Picker<RulesContextPickerDelegate>>,
+}
+
+impl RulesContextPicker {
+    pub fn new(
+        thread_store: WeakEntity<ThreadStore>,
+        context_picker: WeakEntity<ContextPicker>,
+        context_store: WeakEntity<context_store::ContextStore>,
+        window: &mut Window,
+        cx: &mut Context<Self>,
+    ) -> Self {
+        let delegate = RulesContextPickerDelegate::new(thread_store, context_picker, context_store);
+        let picker = cx.new(|cx| Picker::uniform_list(delegate, window, cx));
+
+        RulesContextPicker { picker }
+    }
+}
+
+impl Focusable for RulesContextPicker {
+    fn focus_handle(&self, cx: &App) -> FocusHandle {
+        self.picker.focus_handle(cx)
+    }
+}
+
+impl Render for RulesContextPicker {
+    fn render(&mut self, _window: &mut Window, _cx: &mut Context<Self>) -> impl IntoElement {
+        self.picker.clone()
+    }
+}
+
+#[derive(Debug, Clone)]
+pub struct RulesContextEntry {
+    pub prompt_id: UserPromptId,
+    pub title: SharedString,
+}
+
+pub struct RulesContextPickerDelegate {
+    thread_store: WeakEntity<ThreadStore>,
+    context_picker: WeakEntity<ContextPicker>,
+    context_store: WeakEntity<context_store::ContextStore>,
+    matches: Vec<RulesContextEntry>,
+    selected_index: usize,
+}
+
+impl RulesContextPickerDelegate {
+    pub fn new(
+        thread_store: WeakEntity<ThreadStore>,
+        context_picker: WeakEntity<ContextPicker>,
+        context_store: WeakEntity<context_store::ContextStore>,
+    ) -> Self {
+        RulesContextPickerDelegate {
+            thread_store,
+            context_picker,
+            context_store,
+            matches: Vec::new(),
+            selected_index: 0,
+        }
+    }
+}
+
+impl PickerDelegate for RulesContextPickerDelegate {
+    type ListItem = ListItem;
+
+    fn match_count(&self) -> usize {
+        self.matches.len()
+    }
+
+    fn selected_index(&self) -> usize {
+        self.selected_index
+    }
+
+    fn set_selected_index(
+        &mut self,
+        ix: usize,
+        _window: &mut Window,
+        _cx: &mut Context<Picker<Self>>,
+    ) {
+        self.selected_index = ix;
+    }
+
+    fn placeholder_text(&self, _window: &mut Window, _cx: &mut App) -> Arc<str> {
+        "Search available rules…".into()
+    }
+
+    fn update_matches(
+        &mut self,
+        query: String,
+        window: &mut Window,
+        cx: &mut Context<Picker<Self>>,
+    ) -> Task<()> {
+        let Some(thread_store) = self.thread_store.upgrade() else {
+            return Task::ready(());
+        };
+
+        let search_task = search_rules(query, Arc::new(AtomicBool::default()), thread_store, cx);
+        cx.spawn_in(window, async move |this, cx| {
+            let matches = search_task.await;
+            this.update(cx, |this, cx| {
+                this.delegate.matches = matches;
+                this.delegate.selected_index = 0;
+                cx.notify();
+            })
+            .ok();
+        })
+    }
+
+    fn confirm(&mut self, _secondary: bool, _window: &mut Window, cx: &mut Context<Picker<Self>>) {
+        let Some(entry) = self.matches.get(self.selected_index) else {
+            return;
+        };
+
+        let Some(thread_store) = self.thread_store.upgrade() else {
+            return;
+        };
+
+        let prompt_id = entry.prompt_id;
+
+        let load_rules_task = thread_store.update(cx, |thread_store, cx| {
+            thread_store.load_rules(prompt_id, cx)
+        });
+
+        cx.spawn(async move |this, cx| {
+            let (metadata, text) = load_rules_task.await?;
+            let Some(title) = metadata.title else {
+                return Err(anyhow!("Encountered user rule with no title when attempting to add it to agent context."));
+            };
+            this.update(cx, |this, cx| {
+                this.delegate
+                    .context_store
+                    .update(cx, |context_store, cx| {
+                        context_store.add_rules(prompt_id, title, text, true, cx)
+                    })
+                    .ok();
+            })
+        })
+        .detach_and_log_err(cx);
+    }
+
+    fn dismissed(&mut self, _window: &mut Window, cx: &mut Context<Picker<Self>>) {
+        self.context_picker
+            .update(cx, |_, cx| {
+                cx.emit(DismissEvent);
+            })
+            .ok();
+    }
+
+    fn render_match(
+        &self,
+        ix: usize,
+        selected: bool,
+        _window: &mut Window,
+        cx: &mut Context<Picker<Self>>,
+    ) -> Option<Self::ListItem> {
+        let thread = &self.matches[ix];
+
+        Some(ListItem::new(ix).inset(true).toggle_state(selected).child(
+            render_thread_context_entry(thread, self.context_store.clone(), cx),
+        ))
+    }
+}
+
+pub fn render_thread_context_entry(
+    user_rules: &RulesContextEntry,
+    context_store: WeakEntity<ContextStore>,
+    cx: &mut App,
+) -> Div {
+    let added = context_store.upgrade().map_or(false, |ctx_store| {
+        ctx_store
+            .read(cx)
+            .includes_user_rules(&user_rules.prompt_id)
+            .is_some()
+    });
+
+    h_flex()
+        .gap_1p5()
+        .w_full()
+        .justify_between()
+        .child(
+            h_flex()
+                .gap_1p5()
+                .max_w_72()
+                .child(
+                    Icon::new(RULES_ICON)
+                        .size(IconSize::XSmall)
+                        .color(Color::Muted),
+                )
+                .child(Label::new(user_rules.title.clone()).truncate()),
+        )
+        .when(added, |el| {
+            el.child(
+                h_flex()
+                    .gap_1()
+                    .child(
+                        Icon::new(IconName::Check)
+                            .size(IconSize::Small)
+                            .color(Color::Success),
+                    )
+                    .child(Label::new("Added").size(LabelSize::Small)),
+            )
+        })
+}
+
+pub(crate) fn search_rules(
+    query: String,
+    cancellation_flag: Arc<AtomicBool>,
+    thread_store: Entity<ThreadStore>,
+    cx: &mut App,
+) -> Task<Vec<RulesContextEntry>> {
+    let Some(prompt_store) = thread_store.read(cx).prompt_store() else {
+        return Task::ready(vec![]);
+    };
+    let search_task = prompt_store.read(cx).search(query, cancellation_flag, cx);
+    cx.background_spawn(async move {
+        search_task
+            .await
+            .into_iter()
+            .flat_map(|metadata| {
+                // Default prompts are filtered out as they are automatically included.
+                if metadata.default {
+                    None
+                } else {
+                    match metadata.id {
+                        PromptId::EditWorkflow => None,
+                        PromptId::User { uuid } => Some(RulesContextEntry {
+                            prompt_id: uuid,
+                            title: metadata.title?,
+                        }),
+                    }
+                }
+            })
+            .collect::<Vec<_>>()
+    })
+}
diff --git a/crates/agent/src/context_picker/thread_context_picker.rs b/crates/agent/src/context_picker/thread_context_picker.rs
index 941926a898..030eaf06af 100644
--- a/crates/agent/src/context_picker/thread_context_picker.rs
+++ b/crates/agent/src/context_picker/thread_context_picker.rs
@@ -103,11 +103,11 @@ impl PickerDelegate for ThreadContextPickerDelegate {
         window: &mut Window,
         cx: &mut Context<Picker<Self>>,
     ) -> Task<()> {
-        let Some(threads) = self.thread_store.upgrade() else {
+        let Some(thread_store) = self.thread_store.upgrade() else {
             return Task::ready(());
         };
 
-        let search_task = search_threads(query, Arc::new(AtomicBool::default()), threads, cx);
+        let search_task = search_threads(query, Arc::new(AtomicBool::default()), thread_store, cx);
         cx.spawn_in(window, async move |this, cx| {
             let matches = search_task.await;
             this.update(cx, |this, cx| {
@@ -217,15 +217,15 @@ pub(crate) fn search_threads(
     thread_store: Entity<ThreadStore>,
     cx: &mut App,
 ) -> Task<Vec<ThreadMatch>> {
-    let threads = thread_store.update(cx, |this, _cx| {
-        this.threads()
-            .into_iter()
-            .map(|thread| ThreadContextEntry {
-                id: thread.id,
-                summary: thread.summary,
-            })
-            .collect::<Vec<_>>()
-    });
+    let threads = thread_store
+        .read(cx)
+        .threads()
+        .into_iter()
+        .map(|thread| ThreadContextEntry {
+            id: thread.id,
+            summary: thread.summary,
+        })
+        .collect::<Vec<_>>();
 
     let executor = cx.background_executor().clone();
     cx.background_spawn(async move {
diff --git a/crates/agent/src/context_store.rs b/crates/agent/src/context_store.rs
index a44d0caedf..6045a48a27 100644
--- a/crates/agent/src/context_store.rs
+++ b/crates/agent/src/context_store.rs
@@ -9,6 +9,7 @@ use futures::{self, Future, FutureExt, future};
 use gpui::{App, AppContext as _, Context, Entity, SharedString, Task, WeakEntity};
 use language::{Buffer, File};
 use project::{Project, ProjectItem, ProjectPath, Worktree};
+use prompt_store::UserPromptId;
 use rope::{Point, Rope};
 use text::{Anchor, BufferId, OffsetRangeExt};
 use util::{ResultExt as _, maybe};
@@ -16,7 +17,7 @@ use util::{ResultExt as _, maybe};
 use crate::ThreadStore;
 use crate::context::{
     AssistantContext, ContextBuffer, ContextId, ContextSymbol, ContextSymbolId, DirectoryContext,
-    ExcerptContext, FetchedUrlContext, FileContext, SymbolContext, ThreadContext,
+    ExcerptContext, FetchedUrlContext, FileContext, RulesContext, SymbolContext, ThreadContext,
 };
 use crate::context_strip::SuggestedContext;
 use crate::thread::{Thread, ThreadId};
@@ -25,7 +26,6 @@ pub struct ContextStore {
     project: WeakEntity<Project>,
     context: Vec<AssistantContext>,
     thread_store: Option<WeakEntity<ThreadStore>>,
-    // TODO: If an EntityId is used for all context types (like BufferId), can remove ContextId.
     next_context_id: ContextId,
     files: BTreeMap<BufferId, ContextId>,
     directories: HashMap<ProjectPath, ContextId>,
@@ -35,6 +35,7 @@ pub struct ContextStore {
     threads: HashMap<ThreadId, ContextId>,
     thread_summary_tasks: Vec<Task<()>>,
     fetched_urls: HashMap<String, ContextId>,
+    user_rules: HashMap<UserPromptId, ContextId>,
 }
 
 impl ContextStore {
@@ -55,6 +56,7 @@ impl ContextStore {
             threads: HashMap::default(),
             thread_summary_tasks: Vec::new(),
             fetched_urls: HashMap::default(),
+            user_rules: HashMap::default(),
         }
     }
 
@@ -72,6 +74,7 @@ impl ContextStore {
         self.directories.clear();
         self.threads.clear();
         self.fetched_urls.clear();
+        self.user_rules.clear();
     }
 
     pub fn add_file_from_path(
@@ -390,6 +393,42 @@ impl ContextStore {
         cx.notify();
     }
 
+    pub fn add_rules(
+        &mut self,
+        prompt_id: UserPromptId,
+        title: impl Into<SharedString>,
+        text: impl Into<SharedString>,
+        remove_if_exists: bool,
+        cx: &mut Context<ContextStore>,
+    ) {
+        if let Some(context_id) = self.includes_user_rules(&prompt_id) {
+            if remove_if_exists {
+                self.remove_context(context_id, cx);
+            }
+        } else {
+            self.insert_user_rules(prompt_id, title, text, cx);
+        }
+    }
+
+    pub fn insert_user_rules(
+        &mut self,
+        prompt_id: UserPromptId,
+        title: impl Into<SharedString>,
+        text: impl Into<SharedString>,
+        cx: &mut Context<ContextStore>,
+    ) {
+        let id = self.next_context_id.post_inc();
+
+        self.user_rules.insert(prompt_id, id);
+        self.context.push(AssistantContext::Rules(RulesContext {
+            id,
+            prompt_id,
+            title: title.into(),
+            text: text.into(),
+        }));
+        cx.notify();
+    }
+
     pub fn add_fetched_url(
         &mut self,
         url: String,
@@ -518,6 +557,9 @@ impl ContextStore {
             AssistantContext::Thread(_) => {
                 self.threads.retain(|_, context_id| *context_id != id);
             }
+            AssistantContext::Rules(RulesContext { prompt_id, .. }) => {
+                self.user_rules.remove(&prompt_id);
+            }
         }
 
         cx.notify();
@@ -614,6 +656,10 @@ impl ContextStore {
         self.threads.get(thread_id).copied()
     }
 
+    pub fn includes_user_rules(&self, prompt_id: &UserPromptId) -> Option<ContextId> {
+        self.user_rules.get(prompt_id).copied()
+    }
+
     pub fn includes_url(&self, url: &str) -> Option<ContextId> {
         self.fetched_urls.get(url).copied()
     }
@@ -641,7 +687,8 @@ impl ContextStore {
                 | AssistantContext::Symbol(_)
                 | AssistantContext::Excerpt(_)
                 | AssistantContext::FetchedUrl(_)
-                | AssistantContext::Thread(_) => None,
+                | AssistantContext::Thread(_)
+                | AssistantContext::Rules(_) => None,
             })
             .collect()
     }
@@ -876,6 +923,10 @@ pub fn refresh_context_store_text(
                 // and doing the caching properly could be tricky (unless it's already handled by
                 // the HttpClient?).
                 AssistantContext::FetchedUrl(_) => {}
+                AssistantContext::Rules(user_rules_context) => {
+                    let context_store = context_store.clone();
+                    return Some(refresh_user_rules(context_store, user_rules_context, cx));
+                }
             }
 
             None
@@ -1026,6 +1077,45 @@ fn refresh_thread_text(
     })
 }
 
+fn refresh_user_rules(
+    context_store: Entity<ContextStore>,
+    user_rules_context: &RulesContext,
+    cx: &App,
+) -> Task<()> {
+    let id = user_rules_context.id;
+    let prompt_id = user_rules_context.prompt_id;
+    let Some(thread_store) = context_store.read(cx).thread_store.as_ref() else {
+        return Task::ready(());
+    };
+    let Ok(load_task) = thread_store.read_with(cx, |thread_store, cx| {
+        thread_store.load_rules(prompt_id, cx)
+    }) else {
+        return Task::ready(());
+    };
+    cx.spawn(async move |cx| {
+        if let Ok((metadata, text)) = load_task.await {
+            if let Some(title) = metadata.title.clone() {
+                context_store
+                    .update(cx, |context_store, _cx| {
+                        context_store.replace_context(AssistantContext::Rules(RulesContext {
+                            id,
+                            prompt_id,
+                            title,
+                            text: text.into(),
+                        }));
+                    })
+                    .ok();
+                return;
+            }
+        }
+        context_store
+            .update(cx, |context_store, cx| {
+                context_store.remove_context(id, cx);
+            })
+            .ok();
+    })
+}
+
 fn refresh_context_buffer(
     context_buffer: &ContextBuffer,
     cx: &App,
diff --git a/crates/agent/src/thread.rs b/crates/agent/src/thread.rs
index 061be6f738..9769fd92ba 100644
--- a/crates/agent/src/thread.rs
+++ b/crates/agent/src/thread.rs
@@ -774,7 +774,9 @@ impl Thread {
                                 cx,
                             );
                         }
-                        AssistantContext::FetchedUrl(_) | AssistantContext::Thread(_) => {}
+                        AssistantContext::FetchedUrl(_)
+                        | AssistantContext::Thread(_)
+                        | AssistantContext::Rules(_) => {}
                     }
                 }
             });
diff --git a/crates/agent/src/thread_store.rs b/crates/agent/src/thread_store.rs
index 646a26d26d..1f57c08cc7 100644
--- a/crates/agent/src/thread_store.rs
+++ b/crates/agent/src/thread_store.rs
@@ -24,8 +24,8 @@ use heed::types::SerdeBincode;
 use language_model::{LanguageModelToolUseId, Role, TokenUsage};
 use project::{Project, Worktree};
 use prompt_store::{
-    DefaultUserRulesContext, ProjectContext, PromptBuilder, PromptId, PromptStore,
-    PromptsUpdatedEvent, RulesFileContext, WorktreeContext,
+    ProjectContext, PromptBuilder, PromptId, PromptMetadata, PromptStore, PromptsUpdatedEvent,
+    RulesFileContext, UserPromptId, UserRulesContext, WorktreeContext,
 };
 use serde::{Deserialize, Serialize};
 use settings::{Settings as _, SettingsStore};
@@ -62,6 +62,7 @@ pub struct ThreadStore {
     project: Entity<Project>,
     tools: Entity<ToolWorkingSet>,
     prompt_builder: Arc<PromptBuilder>,
+    prompt_store: Option<Entity<PromptStore>>,
     context_server_manager: Entity<ContextServerManager>,
     context_server_tool_ids: HashMap<Arc<str>, Vec<ToolId>>,
     threads: Vec<SerializedThreadMetadata>,
@@ -135,6 +136,7 @@ impl ThreadStore {
         let (ready_tx, ready_rx) = oneshot::channel();
         let mut ready_tx = Some(ready_tx);
         let reload_system_prompt_task = cx.spawn({
+            let prompt_store = prompt_store.clone();
             async move |thread_store, cx| {
                 loop {
                     let Some(reload_task) = thread_store
@@ -158,6 +160,7 @@ impl ThreadStore {
             project,
             tools,
             prompt_builder,
+            prompt_store,
             context_server_manager,
             context_server_tool_ids: HashMap::default(),
             threads: Vec::new(),
@@ -245,7 +248,7 @@ impl ThreadStore {
             let default_user_rules = default_user_rules
                 .into_iter()
                 .flat_map(|(contents, prompt_metadata)| match contents {
-                    Ok(contents) => Some(DefaultUserRulesContext {
+                    Ok(contents) => Some(UserRulesContext {
                         uuid: match prompt_metadata.id {
                             PromptId::User { uuid } => uuid,
                             PromptId::EditWorkflow => return None,
@@ -346,6 +349,27 @@ impl ThreadStore {
         self.context_server_manager.clone()
     }
 
+    pub fn prompt_store(&self) -> Option<Entity<PromptStore>> {
+        self.prompt_store.clone()
+    }
+
+    pub fn load_rules(
+        &self,
+        prompt_id: UserPromptId,
+        cx: &App,
+    ) -> Task<Result<(PromptMetadata, String)>> {
+        let prompt_id = PromptId::User { uuid: prompt_id };
+        let Some(prompt_store) = self.prompt_store.as_ref() else {
+            return Task::ready(Err(anyhow!("Prompt store unexpectedly missing.")));
+        };
+        let prompt_store = prompt_store.read(cx);
+        let Some(metadata) = prompt_store.metadata(prompt_id) else {
+            return Task::ready(Err(anyhow!("User rules not found in library.")));
+        };
+        let text_task = prompt_store.load(prompt_id, cx);
+        cx.background_spawn(async move { Ok((metadata, text_task.await?)) })
+    }
+
     pub fn tools(&self) -> Entity<ToolWorkingSet> {
         self.tools.clone()
     }
diff --git a/crates/agent/src/ui/context_pill.rs b/crates/agent/src/ui/context_pill.rs
index da07522745..cd5e63bc4f 100644
--- a/crates/agent/src/ui/context_pill.rs
+++ b/crates/agent/src/ui/context_pill.rs
@@ -354,6 +354,16 @@ impl AddedContext {
                     .read(cx)
                     .is_generating_detailed_summary(),
             },
+
+            AssistantContext::Rules(user_rules_context) => AddedContext {
+                id: user_rules_context.id,
+                kind: ContextKind::Rules,
+                name: user_rules_context.title.clone(),
+                parent: None,
+                tooltip: None,
+                icon_path: None,
+                summarizing: false,
+            },
         }
     }
 }
diff --git a/crates/assistant/src/assistant_panel.rs b/crates/assistant/src/assistant_panel.rs
index 4760d4454f..205db386e2 100644
--- a/crates/assistant/src/assistant_panel.rs
+++ b/crates/assistant/src/assistant_panel.rs
@@ -27,7 +27,7 @@ use language_model::{
 };
 use project::Project;
 use prompt_library::{PromptLibrary, open_prompt_library};
-use prompt_store::{PromptBuilder, PromptId};
+use prompt_store::{PromptBuilder, PromptId, UserPromptId};
 
 use search::{BufferSearchBar, buffer_search::DivRegistrar};
 use settings::{Settings, update_settings_file};
@@ -58,11 +58,11 @@ pub fn init(cx: &mut App) {
                 .register_action(AssistantPanel::show_configuration)
                 .register_action(AssistantPanel::create_new_context)
                 .register_action(AssistantPanel::restart_context_servers)
-                .register_action(|workspace, _: &OpenPromptLibrary, window, cx| {
+                .register_action(|workspace, action: &OpenPromptLibrary, window, cx| {
                     if let Some(panel) = workspace.panel::<AssistantPanel>(cx) {
                         workspace.focus_panel::<AssistantPanel>(window, cx);
                         panel.update(cx, |panel, cx| {
-                            panel.deploy_prompt_library(&OpenPromptLibrary::default(), window, cx)
+                            panel.deploy_prompt_library(action, window, cx)
                         });
                     }
                 });
@@ -1060,7 +1060,9 @@ impl AssistantPanel {
                     None,
                 ))
             }),
-            action.prompt_to_focus.map(|uuid| PromptId::User { uuid }),
+            action.prompt_to_select.map(|uuid| PromptId::User {
+                uuid: UserPromptId(uuid),
+            }),
             cx,
         )
         .detach_and_log_err(cx);
diff --git a/crates/assistant_slash_commands/src/prompt_command.rs b/crates/assistant_slash_commands/src/prompt_command.rs
index a057023197..c177f9f359 100644
--- a/crates/assistant_slash_commands/src/prompt_command.rs
+++ b/crates/assistant_slash_commands/src/prompt_command.rs
@@ -44,9 +44,10 @@ impl SlashCommand for PromptSlashCommand {
         let store = PromptStore::global(cx);
         let query = arguments.to_owned().join(" ");
         cx.spawn(async move |cx| {
+            let cancellation_flag = Arc::new(AtomicBool::default());
             let prompts: Vec<PromptMetadata> = store
                 .await?
-                .read_with(cx, |store, cx| store.search(query, cx))?
+                .read_with(cx, |store, cx| store.search(query, cancellation_flag, cx))?
                 .await;
             Ok(prompts
                 .into_iter()
diff --git a/crates/prompt_library/src/prompt_library.rs b/crates/prompt_library/src/prompt_library.rs
index a0e9fbc9a3..d630ae2035 100644
--- a/crates/prompt_library/src/prompt_library.rs
+++ b/crates/prompt_library/src/prompt_library.rs
@@ -16,6 +16,7 @@ use release_channel::ReleaseChannel;
 use rope::Rope;
 use settings::Settings;
 use std::sync::Arc;
+use std::sync::atomic::AtomicBool;
 use std::time::Duration;
 use theme::ThemeSettings;
 use ui::{
@@ -75,7 +76,7 @@ pub fn open_prompt_library(
     language_registry: Arc<LanguageRegistry>,
     inline_assist_delegate: Box<dyn InlineAssistDelegate>,
     make_completion_provider: Arc<dyn Fn() -> Box<dyn CompletionProvider>>,
-    prompt_to_focus: Option<PromptId>,
+    prompt_to_select: Option<PromptId>,
     cx: &mut App,
 ) -> Task<Result<WindowHandle<PromptLibrary>>> {
     let store = PromptStore::global(cx);
@@ -90,8 +91,8 @@ pub fn open_prompt_library(
                 if let Some(existing_window) = existing_window {
                     existing_window
                         .update(cx, |prompt_library, window, cx| {
-                            if let Some(prompt_to_focus) = prompt_to_focus {
-                                prompt_library.load_prompt(prompt_to_focus, true, window, cx);
+                            if let Some(prompt_to_select) = prompt_to_select {
+                                prompt_library.load_prompt(prompt_to_select, true, window, cx);
                             }
                             window.activate_window()
                         })
@@ -126,18 +127,15 @@ pub fn open_prompt_library(
                 },
                 |window, cx| {
                     cx.new(|cx| {
-                        let mut prompt_library = PromptLibrary::new(
+                        PromptLibrary::new(
                             store,
                             language_registry,
                             inline_assist_delegate,
                             make_completion_provider,
+                            prompt_to_select,
                             window,
                             cx,
-                        );
-                        if let Some(prompt_to_focus) = prompt_to_focus {
-                            prompt_library.load_prompt(prompt_to_focus, true, window, cx);
-                        }
-                        prompt_library
+                        )
                     })
                 },
             )
@@ -221,7 +219,8 @@ impl PickerDelegate for PromptPickerDelegate {
         window: &mut Window,
         cx: &mut Context<Picker<Self>>,
     ) -> Task<()> {
-        let search = self.store.read(cx).search(query, cx);
+        let cancellation_flag = Arc::new(AtomicBool::default());
+        let search = self.store.read(cx).search(query, cancellation_flag, cx);
         let prev_prompt_id = self.matches.get(self.selected_index).map(|mat| mat.id);
         cx.spawn_in(window, async move |this, cx| {
             let (matches, selected_index) = cx
@@ -353,13 +352,26 @@ impl PromptLibrary {
         language_registry: Arc<LanguageRegistry>,
         inline_assist_delegate: Box<dyn InlineAssistDelegate>,
         make_completion_provider: Arc<dyn Fn() -> Box<dyn CompletionProvider>>,
+        prompt_to_select: Option<PromptId>,
         window: &mut Window,
         cx: &mut Context<Self>,
     ) -> Self {
+        let (selected_index, matches) = if let Some(prompt_to_select) = prompt_to_select {
+            let matches = store.read(cx).all_prompt_metadata();
+            let selected_index = matches
+                .iter()
+                .enumerate()
+                .find(|(_, metadata)| metadata.id == prompt_to_select)
+                .map_or(0, |(ix, _)| ix);
+            (selected_index, matches)
+        } else {
+            (0, vec![])
+        };
+
         let delegate = PromptPickerDelegate {
             store: store.clone(),
-            selected_index: 0,
-            matches: Vec::new(),
+            selected_index,
+            matches,
         };
 
         let picker = cx.new(|cx| {
diff --git a/crates/prompt_store/src/prompt_store.rs b/crates/prompt_store/src/prompt_store.rs
index 66e4b9072f..84aaa688cd 100644
--- a/crates/prompt_store/src/prompt_store.rs
+++ b/crates/prompt_store/src/prompt_store.rs
@@ -54,14 +54,14 @@ pub struct PromptMetadata {
 #[derive(Clone, Copy, Debug, PartialEq, Eq, Hash, Serialize, Deserialize)]
 #[serde(tag = "kind")]
 pub enum PromptId {
-    User { uuid: Uuid },
+    User { uuid: UserPromptId },
     EditWorkflow,
 }
 
 impl PromptId {
     pub fn new() -> PromptId {
         PromptId::User {
-            uuid: Uuid::new_v4(),
+            uuid: UserPromptId::new(),
         }
     }
 
@@ -70,6 +70,22 @@ impl PromptId {
     }
 }
 
+#[derive(Clone, Copy, Debug, PartialEq, Eq, Hash, Serialize, Deserialize)]
+#[serde(transparent)]
+pub struct UserPromptId(pub Uuid);
+
+impl UserPromptId {
+    pub fn new() -> UserPromptId {
+        UserPromptId(Uuid::new_v4())
+    }
+}
+
+impl From<Uuid> for UserPromptId {
+    fn from(uuid: Uuid) -> Self {
+        UserPromptId(uuid)
+    }
+}
+
 pub struct PromptStore {
     env: heed::Env,
     metadata_cache: RwLock<MetadataCache>,
@@ -212,7 +228,7 @@ impl PromptStore {
 
         for (prompt_id_v1, metadata_v1) in metadata_v1 {
             let prompt_id_v2 = PromptId::User {
-                uuid: prompt_id_v1.0,
+                uuid: UserPromptId(prompt_id_v1.0),
             };
             let Some(body_v1) = bodies_v1.remove(&prompt_id_v1) else {
                 continue;
@@ -257,6 +273,10 @@ impl PromptStore {
         })
     }
 
+    pub fn all_prompt_metadata(&self) -> Vec<PromptMetadata> {
+        self.metadata_cache.read().metadata.clone()
+    }
+
     pub fn default_prompt_metadata(&self) -> Vec<PromptMetadata> {
         return self
             .metadata_cache
@@ -314,7 +334,12 @@ impl PromptStore {
         Some(metadata.id)
     }
 
-    pub fn search(&self, query: String, cx: &App) -> Task<Vec<PromptMetadata>> {
+    pub fn search(
+        &self,
+        query: String,
+        cancellation_flag: Arc<AtomicBool>,
+        cx: &App,
+    ) -> Task<Vec<PromptMetadata>> {
         let cached_metadata = self.metadata_cache.read().metadata.clone();
         let executor = cx.background_executor().clone();
         cx.background_spawn(async move {
@@ -333,7 +358,7 @@ impl PromptStore {
                     &query,
                     false,
                     100,
-                    &AtomicBool::default(),
+                    &cancellation_flag,
                     executor,
                 )
                 .await;
diff --git a/crates/prompt_store/src/prompts.rs b/crates/prompt_store/src/prompts.rs
index 9dd3df3523..35430e8f06 100644
--- a/crates/prompt_store/src/prompts.rs
+++ b/crates/prompt_store/src/prompts.rs
@@ -15,34 +15,32 @@ use std::{
 };
 use text::LineEnding;
 use util::{ResultExt, get_system_shell};
-use uuid::Uuid;
+
+use crate::UserPromptId;
 
 #[derive(Debug, Clone, Serialize)]
 pub struct ProjectContext {
     pub worktrees: Vec<WorktreeContext>,
     /// Whether any worktree has a rules_file. Provided as a field because handlebars can't do this.
     pub has_rules: bool,
-    pub default_user_rules: Vec<DefaultUserRulesContext>,
-    /// `!default_user_rules.is_empty()` - provided as a field because handlebars can't do this.
-    pub has_default_user_rules: bool,
+    pub user_rules: Vec<UserRulesContext>,
+    /// `!user_rules.is_empty()` - provided as a field because handlebars can't do this.
+    pub has_user_rules: bool,
     pub os: String,
     pub arch: String,
     pub shell: String,
 }
 
 impl ProjectContext {
-    pub fn new(
-        worktrees: Vec<WorktreeContext>,
-        default_user_rules: Vec<DefaultUserRulesContext>,
-    ) -> Self {
+    pub fn new(worktrees: Vec<WorktreeContext>, default_user_rules: Vec<UserRulesContext>) -> Self {
         let has_rules = worktrees
             .iter()
             .any(|worktree| worktree.rules_file.is_some());
         Self {
             worktrees,
             has_rules,
-            has_default_user_rules: !default_user_rules.is_empty(),
-            default_user_rules,
+            has_user_rules: !default_user_rules.is_empty(),
+            user_rules: default_user_rules,
             os: std::env::consts::OS.to_string(),
             arch: std::env::consts::ARCH.to_string(),
             shell: get_system_shell(),
@@ -51,8 +49,8 @@ impl ProjectContext {
 }
 
 #[derive(Debug, Clone, Serialize)]
-pub struct DefaultUserRulesContext {
-    pub uuid: Uuid,
+pub struct UserRulesContext {
+    pub uuid: UserPromptId,
     pub title: Option<String>,
     pub contents: String,
 }
@@ -397,6 +395,7 @@ impl PromptBuilder {
 #[cfg(test)]
 mod test {
     use super::*;
+    use uuid::Uuid;
 
     #[test]
     fn test_assistant_system_prompt_renders() {
@@ -408,8 +407,8 @@ mod test {
                 text: "".into(),
             }),
         }];
-        let default_user_rules = vec![DefaultUserRulesContext {
-            uuid: Uuid::nil(),
+        let default_user_rules = vec![UserRulesContext {
+            uuid: UserPromptId(Uuid::nil()),
             title: Some("Rules title".into()),
             contents: "Rules contents".into(),
         }];
diff --git a/crates/zed_actions/src/lib.rs b/crates/zed_actions/src/lib.rs
index 6c1852f882..b420662ebb 100644
--- a/crates/zed_actions/src/lib.rs
+++ b/crates/zed_actions/src/lib.rs
@@ -201,7 +201,7 @@ pub mod assistant {
     #[serde(deny_unknown_fields)]
     pub struct OpenPromptLibrary {
         #[serde(skip)]
-        pub prompt_to_focus: Option<Uuid>,
+        pub prompt_to_select: Option<Uuid>,
     }
 
     impl_action_with_deprecated_aliases!(