diff --git a/crates/agent/src/agent.rs b/crates/agent/src/agent.rs
index 148e60b2bf8..dff6744cdfc 100644
--- a/crates/agent/src/agent.rs
+++ b/crates/agent/src/agent.rs
@@ -553,10 +553,15 @@ impl NativeAgent {
         log::debug!("Creating new NativeAgent");
 
         cx.new(|cx| {
-            let subscriptions = vec![cx.subscribe(
-                &LanguageModelRegistry::global(cx),
-                Self::handle_models_updated_event,
-            )];
+            let subscriptions = vec![
+                cx.subscribe(
+                    &LanguageModelRegistry::global(cx),
+                    Self::handle_models_updated_event,
+                ),
+                // Flush thread content on quit so an in-flight async save
+                // can't leave a thread orphaned ("no thread found with ID").
+                cx.on_app_quit(Self::flush_threads_on_quit),
+            ];
 
             if !cx.has_global::<SkillIndex>() {
                 cx.set_global(SkillIndex::default());
@@ -1765,6 +1770,48 @@ impl NativeAgent {
         });
     }
 
+    /// Commits every non-empty thread's content on shutdown so the async
+    /// `save_thread` losing the race can't leave metadata without content.
+    fn flush_threads_on_quit(
+        &mut self,
+        cx: &mut Context<Self>,
+    ) -> impl Future<Output = ()> + use<> {
+        let database_future = ThreadsDatabase::connect(cx);
+
+        let mut saves = Vec::new();
+        for session in self.sessions.values() {
+            let thread = session.thread.read(cx);
+            if thread.is_empty() {
+                continue;
+            }
+            let Some(state) = self.projects.get(&session.project_id) else {
+                continue;
+            };
+            let folder_paths = PathList::new(
+                &state
+                    .project
+                    .read(cx)
+                    .visible_worktrees(cx)
+                    .map(|worktree| worktree.read(cx).abs_path().to_path_buf())
+                    .collect::<Vec<_>>(),
+            );
+            saves.push((thread.id().clone(), folder_paths, thread.to_db(cx)));
+        }
+
+        async move {
+            let Ok(database) = database_future.await else {
+                return;
+            };
+            for (id, folder_paths, db_thread) in saves {
+                let db_thread = db_thread.await;
+                database
+                    .save_thread(id, db_thread, folder_paths)
+                    .await
+                    .log_err();
+            }
+        }
+    }
+
     fn send_mcp_prompt(
         &self,
         message_id: UserMessageId,
@@ -3749,6 +3796,58 @@ mod internal_tests {
         prompt_task.await.unwrap();
     }
 
+    #[gpui::test]
+    async fn test_threads_flushed_to_database_on_app_quit(cx: &mut TestAppContext) {
+        init_test(cx);
+
+        let (_connection, agent, project, acp_thread) = setup_native_agent_session(cx).await;
+        let session_id = cx.update(|cx| acp_thread.read(cx).session_id().clone());
+        let thread = cx.update(|cx| native_thread_for_session(&agent, &session_id, cx));
+
+        // Give the thread content so it's no longer an empty draft.
+        cx.update(|cx| {
+            let path_style = project.read(cx).path_style(cx);
+            thread.update(cx, |thread, cx| {
+                thread.push_acp_user_block(
+                    UserMessageId::new(),
+                    [acp::ContentBlock::from("hello from the user")],
+                    path_style,
+                    cx,
+                );
+            });
+        });
+        cx.run_until_parked();
+
+        // Reproduce the orphaned state from the bug: the sidebar metadata and
+        // serialized panel still reference the session, but the per-session
+        // async content save never landed, so the content row is absent.
+        let database = cx.update(|cx| ThreadsDatabase::connect(cx)).await.unwrap();
+        database.delete_thread(session_id.clone()).await.unwrap();
+        assert!(
+            database
+                .load_thread(session_id.clone())
+                .await
+                .unwrap()
+                .is_none(),
+            "precondition: content row should be missing before the quit flush"
+        );
+
+        // Quitting must re-commit the content so the thread can be restored.
+        let flush = cx.update(|cx| agent.update(cx, |agent, cx| agent.flush_threads_on_quit(cx)));
+        flush.await;
+
+        let restored = database
+            .load_thread(session_id.clone())
+            .await
+            .unwrap()
+            .expect("thread content should be persisted to the database on quit");
+        assert_eq!(
+            restored.messages.len(),
+            1,
+            "the user message should survive the quit flush"
+        );
+    }
+
     #[test]
     fn test_ambiguous_mcp_prompt_names() {
         // Reserving the built-in `/compact` forces a same-named MCP prompt to be