diff --git a/codex-rs/tui/src/app.rs b/codex-rs/tui/src/app.rs
index 7ed9d0b035..7bbbb2f997 100644
--- a/codex-rs/tui/src/app.rs
+++ b/codex-rs/tui/src/app.rs
@@ -1370,10 +1370,7 @@ impl App {
                                 self.shutdown_current_thread().await;
                                 self.config = resume_config;
                                 tui.set_notification_method(self.config.tui_notification_method);
-                                self.file_search = FileSearchManager::new(
-                                    self.config.cwd.clone(),
-                                    self.app_event_tx.clone(),
-                                );
+                                self.file_search.update_search_dir(self.config.cwd.clone());
                                 let init = self.chatwidget_init_for_forked_or_resumed_thread(
                                     tui,
                                     self.config.clone(),
diff --git a/codex-rs/tui/src/file_search.rs b/codex-rs/tui/src/file_search.rs
index ff55ac1274..90e2f7f149 100644
--- a/codex-rs/tui/src/file_search.rs
+++ b/codex-rs/tui/src/file_search.rs
@@ -38,6 +38,17 @@ impl FileSearchManager {
         }
     }
 
+    /// Updates the directory used for file searches.
+    /// This should be called when the session's CWD changes on resume.
+    /// Drops the current session so it will be recreated with the new directory on next query.
+    pub fn update_search_dir(&mut self, new_dir: PathBuf) {
+        self.search_dir = new_dir;
+        #[expect(clippy::unwrap_used)]
+        let mut st = self.state.lock().unwrap();
+        st.session.take();
+        st.latest_query.clear();
+    }
+
     /// Call whenever the user edits the `@` token.
     pub fn on_user_query(&self, query: String) {
         #[expect(clippy::unwrap_used)]