diff --git a/codex-rs/app-server-protocol/schema/json/ServerNotification.json b/codex-rs/app-server-protocol/schema/json/ServerNotification.json
index e7a533d76b..fab38a9a7e 100644
--- a/codex-rs/app-server-protocol/schema/json/ServerNotification.json
+++ b/codex-rs/app-server-protocol/schema/json/ServerNotification.json
@@ -5115,6 +5115,13 @@
         },
         "turnId": {
           "type": "string"
+        },
+        "windowNumber": {
+          "default": 0,
+          "description": "Current context-window generation. This starts at zero and advances after compaction.",
+          "format": "uint64",
+          "minimum": 0.0,
+          "type": "integer"
         }
       },
       "required": [
diff --git a/codex-rs/app-server-protocol/schema/json/codex_app_server_protocol.schemas.json b/codex-rs/app-server-protocol/schema/json/codex_app_server_protocol.schemas.json
index 53bd7cef4e..c0a4915e5c 100644
--- a/codex-rs/app-server-protocol/schema/json/codex_app_server_protocol.schemas.json
+++ b/codex-rs/app-server-protocol/schema/json/codex_app_server_protocol.schemas.json
@@ -19821,6 +19821,13 @@
           },
           "turnId": {
             "type": "string"
+          },
+          "windowNumber": {
+            "default": 0,
+            "description": "Current context-window generation. This starts at zero and advances after compaction.",
+            "format": "uint64",
+            "minimum": 0.0,
+            "type": "integer"
           }
         },
         "required": [
diff --git a/codex-rs/app-server-protocol/schema/json/codex_app_server_protocol.v2.schemas.json b/codex-rs/app-server-protocol/schema/json/codex_app_server_protocol.v2.schemas.json
index 11540d40c7..7e89da3ac2 100644
--- a/codex-rs/app-server-protocol/schema/json/codex_app_server_protocol.v2.schemas.json
+++ b/codex-rs/app-server-protocol/schema/json/codex_app_server_protocol.v2.schemas.json
@@ -17600,6 +17600,13 @@
         },
         "turnId": {
           "type": "string"
+        },
+        "windowNumber": {
+          "default": 0,
+          "description": "Current context-window generation. This starts at zero and advances after compaction.",
+          "format": "uint64",
+          "minimum": 0.0,
+          "type": "integer"
         }
       },
       "required": [
diff --git a/codex-rs/app-server-protocol/schema/json/v2/ThreadTokenUsageUpdatedNotification.json b/codex-rs/app-server-protocol/schema/json/v2/ThreadTokenUsageUpdatedNotification.json
index 111de85c62..1c213f326b 100644
--- a/codex-rs/app-server-protocol/schema/json/v2/ThreadTokenUsageUpdatedNotification.json
+++ b/codex-rs/app-server-protocol/schema/json/v2/ThreadTokenUsageUpdatedNotification.json
@@ -65,6 +65,13 @@
     },
     "turnId": {
       "type": "string"
+    },
+    "windowNumber": {
+      "default": 0,
+      "description": "Current context-window generation. This starts at zero and advances after compaction.",
+      "format": "uint64",
+      "minimum": 0.0,
+      "type": "integer"
     }
   },
   "required": [
diff --git a/codex-rs/app-server-protocol/schema/typescript/v2/ThreadTokenUsageUpdatedNotification.ts b/codex-rs/app-server-protocol/schema/typescript/v2/ThreadTokenUsageUpdatedNotification.ts
index 1be282500c..6e077945a2 100644
--- a/codex-rs/app-server-protocol/schema/typescript/v2/ThreadTokenUsageUpdatedNotification.ts
+++ b/codex-rs/app-server-protocol/schema/typescript/v2/ThreadTokenUsageUpdatedNotification.ts
@@ -3,4 +3,8 @@
 // This file was generated by [ts-rs](https://github.com/Aleph-Alpha/ts-rs). Do not edit this file manually.
 import type { ThreadTokenUsage } from "./ThreadTokenUsage";
 
-export type ThreadTokenUsageUpdatedNotification = { threadId: string, turnId: string, tokenUsage: ThreadTokenUsage, };
+export type ThreadTokenUsageUpdatedNotification = { threadId: string, turnId: string, tokenUsage: ThreadTokenUsage,
+/**
+ * Current context-window generation. This starts at zero and advances after compaction.
+ */
+windowNumber: number, };
diff --git a/codex-rs/app-server-protocol/src/protocol/v2/thread.rs b/codex-rs/app-server-protocol/src/protocol/v2/thread.rs
index 367a4a64c8..bea41256f5 100644
--- a/codex-rs/app-server-protocol/src/protocol/v2/thread.rs
+++ b/codex-rs/app-server-protocol/src/protocol/v2/thread.rs
@@ -1373,6 +1373,10 @@ pub struct ThreadTokenUsageUpdatedNotification {
     pub thread_id: String,
     pub turn_id: String,
     pub token_usage: ThreadTokenUsage,
+    /// Current context-window generation. This starts at zero and advances after compaction.
+    #[serde(default)]
+    #[ts(type = "number")]
+    pub window_number: u64,
 }
 
 #[derive(Serialize, Deserialize, Debug, Clone, PartialEq, JsonSchema, TS)]
diff --git a/codex-rs/app-server/README.md b/codex-rs/app-server/README.md
index d52f1bd168..3283859050 100644
--- a/codex-rs/app-server/README.md
+++ b/codex-rs/app-server/README.md
@@ -313,7 +313,7 @@ Start a fresh thread when you need a new Codex conversation.
 
 Valid `personality` values are `"friendly"`, `"pragmatic"`, and `"none"`. When `"none"` is selected, the personality placeholder is replaced with an empty string.
 
-To continue a stored session, call `thread/resume` with the `thread.id` you previously recorded. The response shape matches `thread/start`. When the stored session includes persisted token usage, the server emits `thread/tokenUsage/updated` immediately after the response so clients can render restored usage before the next turn starts. You can also pass the same configuration overrides supported by `thread/start`, including `approvalsReviewer`.
+To continue a stored session, call `thread/resume` with the `thread.id` you previously recorded. The response shape matches `thread/start`. When the stored session includes persisted token usage, the server emits `thread/tokenUsage/updated` immediately after the response so clients can render restored usage before the next turn starts. The notification's `windowNumber` is the current zero-based context-window generation, so it also gives the number of compactions in the surviving thread history. You can also pass the same configuration overrides supported by `thread/start`, including `approvalsReviewer`.
 
 By default, `thread/resume` includes the reconstructed turn history in `thread.turns`. Experimental clients can pass `excludeTurns: true` to return only thread metadata and live resume state, then call `thread/turns/list` separately if they want to page the turn history over the network. In that mode the server also skips replaying restored `thread/tokenUsage/updated`, which avoids rebuilding turns just to attribute historical usage.
 
diff --git a/codex-rs/app-server/src/bespoke_event_handling.rs b/codex-rs/app-server/src/bespoke_event_handling.rs
index 863aeac79b..aac1f6dc84 100644
--- a/codex-rs/app-server/src/bespoke_event_handling.rs
+++ b/codex-rs/app-server/src/bespoke_event_handling.rs
@@ -901,8 +901,15 @@ pub(crate) async fn apply_bespoke_event_handling(
                 .await;
         }
         EventMsg::TokenCount(token_count_event) => {
-            handle_token_count_event(conversation_id, event_turn_id, token_count_event, &outgoing)
-                .await;
+            let window_number = conversation.context_window_number().await;
+            handle_token_count_event(
+                conversation_id,
+                event_turn_id,
+                token_count_event,
+                window_number,
+                &outgoing,
+            )
+            .await;
         }
         EventMsg::Error(ev) => {
             thread_watch_manager
@@ -1610,6 +1617,7 @@ async fn handle_token_count_event(
     conversation_id: ThreadId,
     turn_id: String,
     token_count_event: TokenCountEvent,
+    window_number: u64,
     outgoing: &ThreadScopedOutgoingMessageSender,
 ) {
     let TokenCountEvent { info, rate_limits } = token_count_event;
@@ -1618,6 +1626,7 @@ async fn handle_token_count_event(
             thread_id: conversation_id.to_string(),
             turn_id,
             token_usage,
+            window_number,
         };
         outgoing
             .send_server_notification(ServerNotification::ThreadTokenUsageUpdated(notification))
@@ -3829,6 +3838,7 @@ mod tests {
                 info: Some(info),
                 rate_limits: Some(rate_limits),
             },
+            /*window_number*/ 7,
             &outgoing,
         )
         .await;
@@ -3840,6 +3850,7 @@ mod tests {
             ) => {
                 assert_eq!(payload.thread_id, conversation_id.to_string());
                 assert_eq!(payload.turn_id, turn_id);
+                assert_eq!(payload.window_number, 7);
                 let usage = payload.token_usage;
                 assert_eq!(usage.total.total_tokens, 200);
                 assert_eq!(usage.total.cached_input_tokens, 25);
@@ -3886,6 +3897,7 @@ mod tests {
                 info: None,
                 rate_limits: None,
             },
+            /*window_number*/ 0,
             &outgoing,
         )
         .await;
diff --git a/codex-rs/app-server/src/request_processors/token_usage_replay.rs b/codex-rs/app-server/src/request_processors/token_usage_replay.rs
index d4d2228d4b..b12089a239 100644
--- a/codex-rs/app-server/src/request_processors/token_usage_replay.rs
+++ b/codex-rs/app-server/src/request_processors/token_usage_replay.rs
@@ -44,10 +44,12 @@ pub(super) async fn send_thread_token_usage_update_to_connection(
     let Some(info) = conversation.token_usage_info().await else {
         return;
     };
+    let window_number = conversation.context_window_number().await;
     let notification = ThreadTokenUsageUpdatedNotification {
         thread_id: thread_id.to_string(),
         turn_id: token_usage_turn_id.unwrap_or_else(|| latest_token_usage_turn_id(thread)),
         token_usage: ThreadTokenUsage::from(info),
+        window_number,
     };
     outgoing
         .send_server_notification_to_connections(
diff --git a/codex-rs/core/src/codex_thread.rs b/codex-rs/core/src/codex_thread.rs
index c80268e2f9..f04c52b3e9 100644
--- a/codex-rs/core/src/codex_thread.rs
+++ b/codex-rs/core/src/codex_thread.rs
@@ -450,6 +450,11 @@ impl CodexThread {
         self.codex.session.token_usage_info().await
     }
 
+    /// Returns the current context-window generation for this thread.
+    pub async fn context_window_number(&self) -> u64 {
+        self.codex.session.context_window_number().await
+    }
+
     /// Records a user-role session-prefix message without creating a new user turn boundary.
     pub(crate) async fn inject_user_message_without_turn(&self, message: String) {
         let item = ResponseItem::Message {
diff --git a/codex-rs/core/src/session/mod.rs b/codex-rs/core/src/session/mod.rs
index af2412e5c4..f203b53945 100644
--- a/codex-rs/core/src/session/mod.rs
+++ b/codex-rs/core/src/session/mod.rs
@@ -1273,6 +1273,12 @@ impl Session {
         state.token_info()
     }
 
+    /// Returns the current context-window generation for this session.
+    pub(crate) async fn context_window_number(&self) -> u64 {
+        let state = self.state.lock().await;
+        state.auto_compact_window_number()
+    }
+
     pub(crate) async fn get_estimated_token_count(
         &self,
         turn_context: &TurnContext,
@@ -3487,9 +3493,8 @@ impl Session {
     }
 
     pub(crate) async fn current_window_id(&self) -> String {
-        let state = self.state.lock().await;
         let thread_id = self.thread_id;
-        let window_number = state.auto_compact_window_number();
+        let window_number = self.context_window_number().await;
         format!("{thread_id}:{window_number}")
     }
 
diff --git a/codex-rs/exec/tests/event_processor_with_json_output.rs b/codex-rs/exec/tests/event_processor_with_json_output.rs
index 1f44ca31a8..3c26f2272c 100644
--- a/codex-rs/exec/tests/event_processor_with_json_output.rs
+++ b/codex-rs/exec/tests/event_processor_with_json_output.rs
@@ -1239,6 +1239,7 @@ fn token_usage_update_is_emitted_on_turn_completion() {
                     },
                     model_context_window: Some(128_000),
                 },
+                window_number: 0,
             },
         ));
     assert_eq!(
diff --git a/codex-rs/tui/src/app/tests.rs b/codex-rs/tui/src/app/tests.rs
index d8d63575bb..ce25a9fb5b 100644
--- a/codex-rs/tui/src/app/tests.rs
+++ b/codex-rs/tui/src/app/tests.rs
@@ -1135,6 +1135,7 @@ async fn token_usage_update_refreshes_status_line_with_runtime_context_window()
         ThreadId::new(),
         "turn-1",
         Some(950_000),
+        /*window_number*/ 0,
     )));
 
     assert_eq!(
@@ -4651,10 +4652,12 @@ fn token_usage_notification(
     thread_id: ThreadId,
     turn_id: &str,
     model_context_window: Option<i64>,
+    window_number: u64,
 ) -> ServerNotification {
     ServerNotification::ThreadTokenUsageUpdated(ThreadTokenUsageUpdatedNotification {
         thread_id: thread_id.to_string(),
         turn_id: turn_id.to_string(),
+        window_number,
         token_usage: ThreadTokenUsage {
             total: TokenUsageBreakdown {
                 total_tokens: 10,
diff --git a/codex-rs/tui/src/app/thread_events.rs b/codex-rs/tui/src/app/thread_events.rs
index 8d41f1c052..4c090d7eba 100644
--- a/codex-rs/tui/src/app/thread_events.rs
+++ b/codex-rs/tui/src/app/thread_events.rs
@@ -45,6 +45,7 @@ pub(super) struct ThreadEventStore {
     pub(super) pending_interactive_replay: PendingInteractiveReplayState,
     pub(super) active_turn_id: Option<String>,
     pub(super) input_state: Option<ThreadInputState>,
+    latest_token_usage: Option<codex_app_server_protocol::ThreadTokenUsageUpdatedNotification>,
     pub(super) capacity: usize,
     pub(super) active: bool,
 }
@@ -69,6 +70,7 @@ impl ThreadEventStore {
             pending_interactive_replay: PendingInteractiveReplayState::default(),
             active_turn_id: None,
             input_state: None,
+            latest_token_usage: None,
             capacity,
             active: false,
         }
@@ -107,6 +109,9 @@ impl ThreadEventStore {
     pub(super) fn push_notification(&mut self, notification: ServerNotification) {
         self.pending_interactive_replay
             .note_server_notification(&notification);
+        if let ServerNotification::ThreadTokenUsageUpdated(notification) = &notification {
+            self.latest_token_usage = Some(notification.clone());
+        }
         match &notification {
             ServerNotification::TurnStarted(turn) => {
                 self.active_turn_id = Some(turn.turn.id.clone());
@@ -206,6 +211,7 @@ impl ThreadEventStore {
     }
 
     pub(super) fn snapshot(&self) -> ThreadEventSnapshot {
+        let latest_token_usage = self.latest_token_usage.as_ref();
         ThreadEventSnapshot {
             session: self.session.clone(),
             turns: self.turns.clone(),
@@ -218,11 +224,19 @@ impl ThreadEventStore {
                     ThreadBufferedEvent::Request(request) => self
                         .pending_interactive_replay
                         .should_replay_snapshot_request(request),
+                    ThreadBufferedEvent::Notification(
+                        ServerNotification::ThreadTokenUsageUpdated(_),
+                    ) => latest_token_usage.is_none(),
                     ThreadBufferedEvent::Notification(_)
                     | ThreadBufferedEvent::HistoryEntryResponse(_)
                     | ThreadBufferedEvent::FeedbackSubmission(_) => true,
                 })
                 .cloned()
+                .chain(latest_token_usage.cloned().map(|notification| {
+                    ThreadBufferedEvent::Notification(ServerNotification::ThreadTokenUsageUpdated(
+                        notification,
+                    ))
+                }))
                 .collect(),
             input_state: self.input_state.clone(),
         }
@@ -349,6 +363,9 @@ mod tests {
     use codex_app_server_protocol::HookScope as AppServerHookScope;
     use codex_app_server_protocol::HookStartedNotification;
     use codex_app_server_protocol::RequestId as AppServerRequestId;
+    use codex_app_server_protocol::ThreadTokenUsage;
+    use codex_app_server_protocol::ThreadTokenUsageUpdatedNotification;
+    use codex_app_server_protocol::TokenUsageBreakdown;
     use codex_app_server_protocol::TurnCompletedNotification;
     use codex_app_server_protocol::TurnStartedNotification;
     use codex_config::types::ApprovalsReviewer;
@@ -419,6 +436,31 @@ mod tests {
         })
     }
 
+    fn token_usage_notification(thread_id: ThreadId, window_number: u64) -> ServerNotification {
+        ServerNotification::ThreadTokenUsageUpdated(ThreadTokenUsageUpdatedNotification {
+            thread_id: thread_id.to_string(),
+            turn_id: "turn-1".to_string(),
+            window_number,
+            token_usage: ThreadTokenUsage {
+                total: TokenUsageBreakdown {
+                    total_tokens: 10,
+                    input_tokens: 4,
+                    cached_input_tokens: 1,
+                    output_tokens: 5,
+                    reasoning_output_tokens: 0,
+                },
+                last: TokenUsageBreakdown {
+                    total_tokens: 10,
+                    input_tokens: 4,
+                    cached_input_tokens: 1,
+                    output_tokens: 5,
+                    reasoning_output_tokens: 0,
+                },
+                model_context_window: Some(100),
+            },
+        })
+    }
+
     fn hook_started_notification(thread_id: ThreadId, turn_id: &str) -> ServerNotification {
         ServerNotification::HookStarted(HookStartedNotification {
             thread_id: thread_id.to_string(),
@@ -555,6 +597,35 @@ mod tests {
         assert_eq!(store.active_turn_id(), None);
     }
 
+    #[test]
+    fn thread_event_store_snapshot_preserves_latest_token_usage() {
+        let thread_id = ThreadId::new();
+        let mut store = ThreadEventStore::new(/*capacity*/ 1);
+        store.push_notification(token_usage_notification(
+            thread_id, /*window_number*/ 3,
+        ));
+        store.push_notification(ServerNotification::ConfigWarning(
+            codex_app_server_protocol::ConfigWarningNotification {
+                summary: "unrelated warning".to_string(),
+                details: None,
+                path: None,
+                range: None,
+            },
+        ));
+        store.rebase_buffer_after_session_refresh();
+
+        let snapshot = store.snapshot();
+        let [
+            ThreadBufferedEvent::Notification(ServerNotification::ThreadTokenUsageUpdated(
+                notification,
+            )),
+        ] = snapshot.events.as_slice()
+        else {
+            panic!("expected the latest token usage notification");
+        };
+        assert_eq!(notification.window_number, 3);
+    }
+
     #[test]
     fn thread_event_store_rebase_preserves_resolved_request_state() {
         let thread_id = ThreadId::new();
diff --git a/codex-rs/tui/src/chatwidget.rs b/codex-rs/tui/src/chatwidget.rs
index fa745c652e..c1f758f33c 100644
--- a/codex-rs/tui/src/chatwidget.rs
+++ b/codex-rs/tui/src/chatwidget.rs
@@ -551,6 +551,8 @@ pub(crate) struct ChatWidget {
     runtime_model_provider_base_url: Option<String>,
     pub(crate) remote_connection: Option<RemoteConnectionStatus>,
     token_info: Option<TokenUsageInfo>,
+    #[cfg_attr(not(test), allow(dead_code))]
+    window_number: u64,
     rate_limit_snapshots_by_limit_id: BTreeMap<String, RateLimitSnapshotDisplay>,
     refreshing_status_outputs: Vec<(u64, StatusHistoryHandle)>,
     next_status_refresh_request_id: u64,
diff --git a/codex-rs/tui/src/chatwidget/constructor.rs b/codex-rs/tui/src/chatwidget/constructor.rs
index 7fb6fe54e9..a34a118aba 100644
--- a/codex-rs/tui/src/chatwidget/constructor.rs
+++ b/codex-rs/tui/src/chatwidget/constructor.rs
@@ -123,6 +123,7 @@ impl ChatWidget {
             runtime_model_provider_base_url,
             remote_connection: None,
             token_info: None,
+            window_number: 0,
             rate_limit_snapshots_by_limit_id: BTreeMap::new(),
             refreshing_status_outputs: Vec::new(),
             next_status_refresh_request_id: 0,
diff --git a/codex-rs/tui/src/chatwidget/protocol.rs b/codex-rs/tui/src/chatwidget/protocol.rs
index 0c5b0ed3ee..47a71e6407 100644
--- a/codex-rs/tui/src/chatwidget/protocol.rs
+++ b/codex-rs/tui/src/chatwidget/protocol.rs
@@ -30,6 +30,7 @@ impl ChatWidget {
         }
         match notification {
             ServerNotification::ThreadTokenUsageUpdated(notification) => {
+                self.window_number = notification.window_number;
                 self.set_token_info(Some(token_usage_info_from_app_server(
                     notification.token_usage,
                 )));
diff --git a/codex-rs/tui/src/chatwidget/session_flow.rs b/codex-rs/tui/src/chatwidget/session_flow.rs
index 177700d4f4..99fdf79228 100644
--- a/codex-rs/tui/src/chatwidget/session_flow.rs
+++ b/codex-rs/tui/src/chatwidget/session_flow.rs
@@ -27,6 +27,7 @@ impl ChatWidget {
         }
         self.refresh_plan_mode_nudge();
         self.turn_lifecycle.reset_thread();
+        self.window_number = 0;
         self.clear_safety_buffering();
         self.thread_name = session.thread_name.clone();
         self.current_goal_status_indicator = None;
diff --git a/codex-rs/tui/src/chatwidget/tests/helpers.rs b/codex-rs/tui/src/chatwidget/tests/helpers.rs
index 5f890ab000..d9d64a003c 100644
--- a/codex-rs/tui/src/chatwidget/tests/helpers.rs
+++ b/codex-rs/tui/src/chatwidget/tests/helpers.rs
@@ -382,6 +382,14 @@ fn token_usage_breakdown(usage: TokenUsage) -> codex_app_server_protocol::TokenU
 }
 
 pub(super) fn handle_token_count(chat: &mut ChatWidget, info: Option<TokenUsageInfo>) {
+    handle_token_count_with_window_number(chat, info, /*window_number*/ 0);
+}
+
+pub(super) fn handle_token_count_with_window_number(
+    chat: &mut ChatWidget,
+    info: Option<TokenUsageInfo>,
+    window_number: u64,
+) {
     match info {
         Some(info) => {
             chat.handle_server_notification(
@@ -393,6 +401,7 @@ pub(super) fn handle_token_count(chat: &mut ChatWidget, info: Option<TokenUsageI
                             .last_turn_id
                             .clone()
                             .unwrap_or_else(|| "turn-1".to_string()),
+                        window_number,
                         token_usage: codex_app_server_protocol::ThreadTokenUsage {
                             total: token_usage_breakdown(info.total_token_usage),
                             last: token_usage_breakdown(info.last_token_usage),
diff --git a/codex-rs/tui/src/chatwidget/tests/status_and_layout.rs b/codex-rs/tui/src/chatwidget/tests/status_and_layout.rs
index d118191390..f4117e08fb 100644
--- a/codex-rs/tui/src/chatwidget/tests/status_and_layout.rs
+++ b/codex-rs/tui/src/chatwidget/tests/status_and_layout.rs
@@ -41,6 +41,21 @@ async fn token_count_none_resets_context_indicator() {
     assert_eq!(chat.bottom_pane.context_window_percent(), None);
 }
 
+#[tokio::test]
+async fn token_count_updates_context_window_generation() {
+    let (mut chat, _rx, _ops) = make_chatwidget_manual(/*model_override*/ None).await;
+
+    handle_token_count_with_window_number(
+        &mut chat,
+        Some(make_token_info(
+            /*total_tokens*/ 1, /*context_window*/ 100,
+        )),
+        /*window_number*/ 3,
+    );
+
+    assert_eq!(chat.window_number, 3);
+}
+
 #[tokio::test]
 async fn app_server_cyber_policy_error_renders_dedicated_notice() {
     let (mut chat, mut rx, _ops) = make_chatwidget_manual(/*model_override*/ None).await;