diff --git a/codex-rs/app-server/src/codex_message_processor.rs b/codex-rs/app-server/src/codex_message_processor.rs
index 716559e94..d897350bf 100644
--- a/codex-rs/app-server/src/codex_message_processor.rs
+++ b/codex-rs/app-server/src/codex_message_processor.rs
@@ -1921,6 +1921,10 @@ impl CodexMessageProcessor {
         }
     }
 
+    pub(crate) async fn clear_all_thread_listeners(&self) {
+        self.thread_state_manager.clear_all_listeners().await;
+    }
+
     pub(crate) async fn shutdown_threads(&self) {
         let report = self
             .thread_manager
diff --git a/codex-rs/app-server/src/in_process.rs b/codex-rs/app-server/src/in_process.rs
index 3a9286a5f..286210e6e 100644
--- a/codex-rs/app-server/src/in_process.rs
+++ b/codex-rs/app-server/src/in_process.rs
@@ -484,9 +484,10 @@ fn start_uninitialized(args: InProcessStartArgs) -> InProcessClientHandle {
             }
 
             processor.clear_runtime_references();
+            processor.connection_closed(IN_PROCESS_CONNECTION_ID).await;
+            processor.clear_all_thread_listeners().await;
             processor.drain_background_tasks().await;
             processor.shutdown_threads().await;
-            processor.connection_closed(IN_PROCESS_CONNECTION_ID).await;
         });
         let mut pending_request_responses =
             HashMap::<RequestId, oneshot::Sender<PendingClientRequestResponse>>::new();
diff --git a/codex-rs/app-server/src/message_processor.rs b/codex-rs/app-server/src/message_processor.rs
index e16e2e693..5eda1edeb 100644
--- a/codex-rs/app-server/src/message_processor.rs
+++ b/codex-rs/app-server/src/message_processor.rs
@@ -456,6 +456,12 @@ impl MessageProcessor {
         self.codex_message_processor.drain_background_tasks().await;
     }
 
+    pub(crate) async fn clear_all_thread_listeners(&self) {
+        self.codex_message_processor
+            .clear_all_thread_listeners()
+            .await;
+    }
+
     pub(crate) async fn shutdown_threads(&self) {
         self.codex_message_processor.shutdown_threads().await;
     }
diff --git a/codex-rs/app-server/src/thread_state.rs b/codex-rs/app-server/src/thread_state.rs
index 5176fe133..a875a9149 100644
--- a/codex-rs/app-server/src/thread_state.rs
+++ b/codex-rs/app-server/src/thread_state.rs
@@ -196,6 +196,29 @@ impl ThreadStateManager {
         }
     }
 
+    pub(crate) async fn clear_all_listeners(&self) {
+        let thread_states = {
+            let state = self.state.lock().await;
+            state
+                .threads
+                .iter()
+                .map(|(thread_id, thread_entry)| (*thread_id, thread_entry.state.clone()))
+                .collect::<Vec<_>>()
+        };
+
+        for (thread_id, thread_state) in thread_states {
+            let mut thread_state = thread_state.lock().await;
+            tracing::debug!(
+                thread_id = %thread_id,
+                listener_generation = thread_state.listener_generation,
+                had_listener = thread_state.cancel_tx.is_some(),
+                had_active_turn = thread_state.active_turn_snapshot().is_some(),
+                "clearing thread listener during app-server shutdown"
+            );
+            thread_state.clear_listener();
+        }
+    }
+
     pub(crate) async fn unsubscribe_connection_from_thread(
         &self,
         thread_id: ThreadId,