diff --git a/packages/server/src/server/agent/agent-manager.test.ts b/packages/server/src/server/agent/agent-manager.test.ts
index 1ff1b1933..d55f1c598 100644
--- a/packages/server/src/server/agent/agent-manager.test.ts
+++ b/packages/server/src/server/agent/agent-manager.test.ts
@@ -4757,7 +4757,7 @@ test("replaceAgentRun stays running when a stale old terminal arrives before the
   unsubscribe();
 });
 
-test("applies live autonomous events while no foreground run is active", async () => {
+test("applies live autonomous events and preserves usage omitted from completion", async () => {
   const workdir = mkdtempSync(join(tmpdir(), "agent-manager-live-events-"));
   const storagePath = join(workdir, "agents");
   const storage = new AgentStorage(storagePath, logger);
@@ -4816,6 +4816,16 @@ test("applies live autonomous events while no foreground run is active", async (
     provider: "codex",
     turnId: autonomousTurnId,
   });
+  capturedSession!.pushEvent({
+    type: "usage_updated",
+    provider: "codex",
+    usage: {
+      inputTokens: 10,
+      contextWindowMaxTokens: 200_000,
+      contextWindowUsedTokens: 175,
+    },
+    turnId: autonomousTurnId,
+  });
   capturedSession!.pushEvent({
     type: "timeline",
     provider: "codex",
@@ -4831,6 +4841,11 @@ test("applies live autonomous events while no foreground run is active", async (
 
   const updated = manager.getAgent(snapshot.id);
   expect(updated?.lifecycle).toBe("idle");
+  expect(updated?.lastUsage).toEqual({
+    inputTokens: 10,
+    contextWindowMaxTokens: 200_000,
+    contextWindowUsedTokens: 175,
+  });
   expect(manager.getTimeline(snapshot.id)).toContainEqual({
     type: "assistant_message",
     text: "AUTONOMOUS_PUMP_MESSAGE",
diff --git a/packages/server/src/server/agent/agent-manager.ts b/packages/server/src/server/agent/agent-manager.ts
index e6c4e68a8..c18e8c902 100644
--- a/packages/server/src/server/agent/agent-manager.ts
+++ b/packages/server/src/server/agent/agent-manager.ts
@@ -3552,7 +3552,12 @@ export class AgentManager {
       },
       "agent.manager.turn.completed",
     );
-    agent.lastUsage = event.usage;
+    if (event.usage) {
+      agent.lastUsage = { ...agent.lastUsage, ...event.usage };
+    }
+    // If no usage on turn_completed, keep lastUsage as-is so context window
+    // data accumulated during streaming isn't lost when the provider omits
+    // it from the completion event.
     agent.lastError = undefined;
     if (!isForegroundEvent && agent.lifecycle !== "idle" && !agent.pendingReplacement) {
       (agent as ActiveManagedAgent).lifecycle = "idle";