diff --git a/codex-rs/tui/src/resume_picker.rs b/codex-rs/tui/src/resume_picker.rs
index 655c0abd9a..c7be652f85 100644
--- a/codex-rs/tui/src/resume_picker.rs
+++ b/codex-rs/tui/src/resume_picker.rs
@@ -477,6 +477,9 @@ async fn run_session_picker_with_loader(
                             return Ok(sel);
                         }
                     }
+                    TuiEvent::Paste(pasted) => {
+                        state.handle_paste(pasted);
+                    }
                     TuiEvent::Draw | TuiEvent::Resize => {
                         if let Ok(size) = alt.tui.terminal.size() {
                             let list_height =
@@ -489,7 +492,6 @@ async fn run_session_picker_with_loader(
                             state.open_pending_transcript_if_ready();
                         }
                     }
-                    _ => {}
                 }
             }
             Some(event) = background_events.next() => {
@@ -543,6 +545,11 @@ fn picker_cwd_filter(
     }
 }
 
+fn normalize_pasted_query(pasted: &str) -> Option<String> {
+    let normalized = pasted.split_whitespace().collect::<Vec<_>>().join(" ");
+    (!normalized.is_empty()).then_some(normalized)
+}
+
 fn spawn_app_server_page_loader(
     app_server: AppServerSession,
     include_non_interactive: bool,
@@ -1227,6 +1234,21 @@ impl PickerState {
         Ok(None)
     }
 
+    fn handle_paste(&mut self, pasted: String) {
+        if self.is_transcript_loading() {
+            return;
+        }
+        let Some(pasted) = normalize_pasted_query(&pasted) else {
+            return;
+        };
+        let mut new_query = self.query.clone();
+        if !new_query.is_empty() && !new_query.ends_with(char::is_whitespace) {
+            new_query.push(' ');
+        }
+        new_query.push_str(&pasted);
+        self.set_query(new_query);
+    }
+
     fn start_initial_load(&mut self) {
         self.relative_time_reference = Some(Utc::now());
         self.reset_pagination();
@@ -6218,6 +6240,87 @@ session_picker_view = "dense"
         assert!(state.pagination.reached_scan_cap);
     }
 
+    #[tokio::test]
+    async fn paste_appends_to_existing_query() {
+        let loader = page_only_loader(|_| {});
+        let mut state = PickerState::new(
+            FrameRequester::test_dummy(),
+            loader,
+            ProviderFilter::MatchDefault(String::from("openai")),
+            /*show_all*/ true,
+            /*filter_cwd*/ None,
+            SessionPickerAction::Resume,
+        );
+        state.query = String::from("resize");
+
+        state.handle_paste(String::from("results"));
+
+        assert_eq!(state.query, "resize results");
+    }
+
+    #[test]
+    fn normalize_pasted_query_collapses_whitespace() {
+        assert_eq!(
+            normalize_pasted_query("  alpha\n\tbeta\r\n gamma  "),
+            Some(String::from("alpha beta gamma"))
+        );
+    }
+
+    #[tokio::test]
+    async fn whitespace_only_paste_is_ignored() {
+        let loader = page_only_loader(|_| {});
+        let mut state = PickerState::new(
+            FrameRequester::test_dummy(),
+            loader,
+            ProviderFilter::MatchDefault(String::from("openai")),
+            /*show_all*/ true,
+            /*filter_cwd*/ None,
+            SessionPickerAction::Resume,
+        );
+        state.query = String::from("resize");
+
+        state.handle_paste(String::from("  \n\t  "));
+
+        assert_eq!(state.query, "resize");
+    }
+
+    #[tokio::test]
+    async fn paste_uses_existing_search_loading_path() {
+        let recorded_requests: Arc<Mutex<Vec<PageLoadRequest>>> = Arc::new(Mutex::new(Vec::new()));
+        let request_sink = recorded_requests.clone();
+        let loader = page_only_loader(move |req: PageLoadRequest| {
+            request_sink.lock().unwrap().push(req);
+        });
+
+        let mut state = PickerState::new(
+            FrameRequester::test_dummy(),
+            loader,
+            ProviderFilter::MatchDefault(String::from("openai")),
+            /*show_all*/ true,
+            /*filter_cwd*/ None,
+            SessionPickerAction::Resume,
+        );
+        state.reset_pagination();
+        state.ingest_page(page(
+            vec![make_row(
+                "/tmp/start.jsonl",
+                "2025-01-01T00:00:00Z",
+                "alpha",
+            )],
+            Some("2025-01-02T00:00:00Z"),
+            /*num_scanned_files*/ 1,
+            /*reached_scan_cap*/ false,
+        ));
+        recorded_requests.lock().unwrap().clear();
+
+        state.handle_paste(String::from("target"));
+
+        let guard = recorded_requests.lock().unwrap();
+        assert_eq!(state.query, "target");
+        assert_eq!(guard.len(), 1);
+        assert!(guard[0].search_token.is_some());
+    }
+
     #[tokio::test]
     async fn esc_with_empty_query_starts_fresh() {
         let loader = page_only_loader(|_| {});