diff --git a/apps/server/src/orchestration-v2/Orchestrator.ts b/apps/server/src/orchestration-v2/Orchestrator.ts
index e199decf35260..bcec0a13cf20a 100644
--- a/apps/server/src/orchestration-v2/Orchestrator.ts
+++ b/apps/server/src/orchestration-v2/Orchestrator.ts
@@ -3454,6 +3454,19 @@ const makeOrchestrator = Effect.fn("orchestrationV2.Orchestrator.layer")(functio
     }
     if (command.type === "thread.settle") {
       const projection = yield* loadProjectionForCommand(command, ["runs", "runtimeRequests"]);
+      if (
+        command.expectedLatestRunId !== undefined &&
+        projection.runs.reduce<OrchestrationV2Run | undefined>(
+          (latest, run) => (latest === undefined || run.ordinal > latest.ordinal ? run : latest),
+          undefined,
+        )?.id !== command.expectedLatestRunId
+      ) {
+        return yield* new OrchestratorDispatchError({
+          commandId: command.commandId,
+          commandType: command.type,
+          cause: "The thread received another run before settlement.",
+        });
+      }
       const queuedMessages = yield* projectionStore
         .getMessagesById(
           command.threadId,
diff --git a/apps/server/src/orchestration-v2/ThreadManagementService.test.ts b/apps/server/src/orchestration-v2/ThreadManagementService.test.ts
index 9285f72d46f56..742616f27bd3e 100644
--- a/apps/server/src/orchestration-v2/ThreadManagementService.test.ts
+++ b/apps/server/src/orchestration-v2/ThreadManagementService.test.ts
@@ -559,28 +559,108 @@ it.effect.each(["live", "no-session", "unsupported-runtime"] as const)(
 );
 
 it.effect.each([
-  { status: "completed" as const, settles: true },
-  { status: "failed" as const, settles: false },
-  { status: "interrupted" as const, settles: false },
-])("settleAfterRun settles only when the run $status", ({ status, settles }) =>
+  { status: "completed" as const, followUp: "none", settles: true },
+  { status: "failed" as const, followUp: "none", settles: false },
+  { status: "interrupted" as const, followUp: "none", settles: false },
+  { status: "completed" as const, followUp: "notification", settles: true },
+  { status: "completed" as const, followUp: "replayed-notification", settles: true },
+  { status: "completed" as const, followUp: "delegated", settles: true },
+  { status: "completed" as const, followUp: "failed-notification", settles: false },
+  { status: "completed" as const, followUp: "held-notification", settles: true },
+  { status: "completed" as const, followUp: "user", settles: false },
+  { status: "completed" as const, followUp: "steered-notification", settles: false },
+])("settleAfterRun handles $status with $followUp follow-up", ({ status, followUp, settles }) =>
   Effect.gen(function* () {
     const projectId = ProjectId.make("project:thread-management:settle-after-run");
     const threadId = ThreadId.make("thread:thread-management:settle-after-run");
     const runId = RunId.make("run:thread-management:settle-after-run");
+    const followUpId = RunId.make(`${runId}:follow-up`);
+    const subscribed = yield* Deferred.make<void>();
+    const events = yield* Queue.unbounded<OrchestrationV2StoredEvent>();
+    const replayRejected = yield* Deferred.make<void>();
+    let sequence = 0;
+    let sequenceReads = 0;
+    let rejectedCommandId: CommandId | undefined;
+    const runs = [{ id: runId, ordinal: 1, status, userMessageId: MessageId.make("original") }];
+    const nextRun = {
+      id: followUpId,
+      ordinal: 2,
+      status: "running" as OrchestrationV2Run["status"],
+      userMessageId: MessageId.make("follow-up"),
+    };
     const dispatched: Array<string> = [];
+    // The notification starts after the completed run was observed, before settlement commits.
+    let raced = false;
     const layerTest = ThreadManagementService.layer.pipe(
       Layer.provide(Layer.mock(ProviderSessionManager.ProviderSessionManagerV2)({})),
       Layer.provide(
         Layer.mock(Orchestrator.OrchestratorV2)({
-          getThreadEventSequence: () => Effect.succeed(0),
+          getThreadEventSequence: () =>
+            Effect.sync(() => {
+              if (followUp === "replayed-notification" && sequenceReads++ === 2) sequence = 1;
+              return sequence;
+            }),
           restartContinuationPending: () => Effect.succeed(false),
-          getThreadRecords: () =>
-            Effect.succeed({
-              thread: { id: threadId, projectId, deletedAt: null },
-              runs: [{ id: runId, status }],
-            } as unknown as OrchestrationV2ThreadProjection),
+          streamStoredEventsFrom: () =>
+            Stream.fromEffect(Deferred.succeed(subscribed, undefined)).pipe(
+              Stream.drain,
+              Stream.concat(Stream.fromQueue(events)),
+            ),
+          getThreadRecords: (_threadId, _fields, filter) =>
+            Effect.sync(
+              () =>
+                ({
+                  thread: { id: threadId, projectId, deletedAt: null },
+                  runs: raced ? [...runs, nextRun] : runs,
+                  messages: [
+                    { id: MessageId.make("original"), runId, role: "user" as const },
+                    {
+                      id: nextRun.userMessageId,
+                      runId: followUpId,
+                      role: "user" as const,
+                      ...(followUp.endsWith("notification") ? { notification: {} } : {}),
+                      ...(followUp === "delegated" ? { delegatedCompletion: {} } : {}),
+                    },
+                    { id: MessageId.make("reply"), runId: followUpId, role: "assistant" as const },
+                    ...(followUp === "steered-notification"
+                      ? [
+                          {
+                            id: MessageId.make("user-steer"),
+                            runId: followUpId,
+                            role: "user" as const,
+                          },
+                        ]
+                      : []),
+                  ].filter(
+                    (message) =>
+                      (filter?.messageIds === undefined ||
+                        filter.messageIds.includes(message.id)) &&
+                      (filter?.messageRunIds === undefined ||
+                        filter.messageRunIds.includes(message.runId)) &&
+                      (filter?.messageRoles === undefined ||
+                        filter.messageRoles.includes(message.role)),
+                  ),
+                }) as unknown as OrchestrationV2ThreadProjection,
+            ),
           dispatch: (command) =>
-            Effect.sync(() => {
+            Effect.gen(function* () {
+              if (followUp !== "none" && !raced) {
+                raced = true;
+                rejectedCommandId = command.commandId;
+                return yield* new Orchestrator.OrchestratorDispatchError({
+                  commandId: command.commandId,
+                  commandType: command.type,
+                  cause: "Thread is still running",
+                });
+              }
+              if (followUp === "replayed-notification" && command.commandId === rejectedCommandId) {
+                yield* Deferred.succeed(replayRejected, undefined);
+                return yield* new Orchestrator.OrchestratorCommandPreviouslyRejectedError({
+                  commandId: command.commandId,
+                  commandType: command.type,
+                  detail: "Thread is still running",
+                });
+              }
               dispatched.push(command.type);
               return { sequence: 1, storedEvents: [] } as never;
             }),
@@ -592,9 +672,33 @@ it.effect.each([
     const service = yield* ThreadManagementService.ThreadManagementService.pipe(
       Effect.provide(layerTest),
     );
-
-    yield* service.settleAfterRun({ projectId, threadId, runId });
-
+    const fiber = yield* service
+      .settleAfterRun({ projectId, threadId, runId })
+      .pipe(Effect.forkChild);
+    if (followUp !== "none") {
+      yield* Deferred.await(subscribed);
+      expect(dispatched).toEqual([]);
+      nextRun.status =
+        followUp === "failed-notification"
+          ? "failed"
+          : followUp === "held-notification"
+            ? "queued"
+            : "completed";
+      yield* Queue.offer(events, {
+        sequence: 1,
+        event: { type: "run.updated", threadId, payload: nextRun },
+      } as unknown as OrchestrationV2StoredEvent);
+    }
+    if (followUp === "replayed-notification") {
+      yield* Deferred.await(replayRejected);
+      expect(dispatched).toEqual([]);
+      sequence = 2;
+      yield* Queue.offer(events, {
+        sequence,
+        event: { type: "run.updated", threadId, payload: nextRun },
+      } as unknown as OrchestrationV2StoredEvent);
+    }
+    yield* Fiber.join(fiber);
     expect(dispatched).toEqual(settles ? ["thread.settle"] : []);
   }),
 );
diff --git a/apps/server/src/orchestration-v2/ThreadManagementService.ts b/apps/server/src/orchestration-v2/ThreadManagementService.ts
index b6c1e27120ae8..46ea454310554 100644
--- a/apps/server/src/orchestration-v2/ThreadManagementService.ts
+++ b/apps/server/src/orchestration-v2/ThreadManagementService.ts
@@ -446,8 +446,8 @@ export interface ThreadManagementServiceShape {
   readonly waitForThread: (
     input: ThreadManagementWaitInput,
   ) => Effect.Effect<ThreadManagementWaitResult, ThreadManagementError>;
-  /** Waits for the agent's run to end before settling its thread and stopping the session.
-   * Other endings or settle refusals leave the thread active. */
+  /** Waits for the agent's run and automatic follow-ups before settling.
+   * A new user turn or an unsuccessful ending leaves the thread active. */
   readonly settleAfterRun: (input: {
     readonly projectId: ProjectId;
     readonly threadId: ThreadId;
@@ -1044,11 +1044,74 @@ const make = Effect.gen(function* () {
   )(function* (input) {
     const { run } = yield* waitForThread({ ...input, timeoutMs: SETTLE_AFTER_RUN_WAIT_MS });
     if (run?.status !== "completed") return;
-    yield* dispatch({
-      type: "thread.settle",
-      commandId: CommandId.make(`server:settle-after-run:${input.runId}`),
-      threadId: input.threadId,
+    const afterSequence = yield* orchestrator.getThreadEventSequence(input.threadId);
+    const trySettle = Effect.gen(function* () {
+      const sequence = yield* orchestrator.getThreadEventSequence(input.threadId);
+      const records = yield* getProjectThreadRecords(input, ["runs"]);
+      const following = records.runs.filter((candidate) => candidate.ordinal > run.ordinal);
+      if (following.length > 0) {
+        const { messages } = yield* getProjectThreadRecords(input, ["messages"], {
+          messageRunIds: following.map((candidate) => candidate.id),
+          messageRoles: ["user"],
+        });
+        const automaticMessageIds = new Set(
+          messages
+            .filter(
+              (message) =>
+                message.role === "user" &&
+                (message.notification !== undefined || message.delegatedCompletion !== undefined),
+            )
+            .map((message) => message.id),
+        );
+        if (
+          messages.some((message) => !automaticMessageIds.has(message.id)) ||
+          following.some((candidate) => !automaticMessageIds.has(candidate.userMessageId))
+        ) {
+          return true;
+        }
+        if (
+          following.some(
+            (candidate) => candidate.status !== "queued" && !isTerminalRunStatus(candidate.status),
+          )
+        )
+          return false;
+        if (
+          following.some(
+            (candidate) => candidate.status !== "queued" && candidate.status !== "completed",
+          )
+        )
+          return true;
+      }
+      const latest = latestRun(records);
+      if (latest === undefined) return true;
+      return yield* dispatch({
+        type: "thread.settle",
+        commandId: CommandId.make(`server:settle-after-run:${input.runId}:${sequence}`),
+        threadId: input.threadId,
+        expectedLatestRunId: latest.id,
+      }).pipe(
+        Effect.as(true),
+        // A notification can start between the projection read and the guarded dispatch.
+        Effect.catchTags({
+          OrchestratorDispatchError: () => Effect.succeed(false),
+          OrchestratorCommandPreviouslyRejectedError: () => Effect.succeed(false),
+        }),
+      );
     });
+    yield* Stream.fromEffect(trySettle).pipe(
+      Stream.concat(
+        orchestrator
+          .streamStoredEventsFrom({
+            threadId: input.threadId,
+            afterSequence,
+            eventType: "run.updated",
+          })
+          .pipe(Stream.mapEffect(() => trySettle)),
+      ),
+      Stream.filter((done) => done),
+      Stream.runHead,
+      Effect.timeoutOption(Duration.millis(SETTLE_AFTER_RUN_WAIT_MS)),
+    );
   });
 
   const settleThread: ThreadManagementServiceShape["settleThread"] = Effect.fn(
diff --git a/apps/server/src/orchestration-v2/runtimeLayer.test.ts b/apps/server/src/orchestration-v2/runtimeLayer.test.ts
index af95d71e6121b..b90f491dfa94e 100644
--- a/apps/server/src/orchestration-v2/runtimeLayer.test.ts
+++ b/apps/server/src/orchestration-v2/runtimeLayer.test.ts
@@ -4859,11 +4859,29 @@ it.layer(layerTest)("OrchestrationV2LayerLive lifecycle", (it) => {
           });
         });
       yield* holdQueueAfterRestart("settle-automatic-restart");
+      const beforeSettle = yield* orchestrator.getThreadProjection(threadId);
+      const oldestRun = beforeSettle.runs.reduce((oldest, run) =>
+        run.ordinal < oldest.ordinal ? run : oldest,
+      );
+      const latestRun = beforeSettle.runs.reduce((latest, run) =>
+        run.ordinal > latest.ordinal ? run : latest,
+      );
+      const staleSettle = yield* orchestrator
+        .dispatch({
+          type: "thread.settle",
+          commandId: CommandId.make("settle-automatic-stale"),
+          threadId,
+          expectedLatestRunId: oldestRun.id,
+        })
+        .pipe(Effect.flip);
+      assert.equal(staleSettle._tag, "OrchestratorDispatchError");
+      assert.isNull((yield* orchestrator.getThreadProjection(threadId)).thread.settledAt);
 
       yield* orchestrator.dispatch({
         type: "thread.settle",
         commandId: CommandId.make("settle-automatic-settle"),
         threadId,
+        expectedLatestRunId: latestRun.id,
       });
       const settled = yield* orchestrator.getThreadProjection(threadId);
       assert.isNotNull(settled.thread.settledAt);
diff --git a/packages/contracts/src/orchestrationV2.ts b/packages/contracts/src/orchestrationV2.ts
index 8234864349504..461ec5e4b3f3e 100644
--- a/packages/contracts/src/orchestrationV2.ts
+++ b/packages/contracts/src/orchestrationV2.ts
@@ -2975,6 +2975,7 @@ export const OrchestrationV2Command = Schema.Union([
     type: Schema.Literal("thread.settle"),
     commandId: CommandId,
     threadId: ThreadId,
+    expectedLatestRunId: Schema.optional(RunId),
     settledAt: Schema.optional(Schema.DateTimeUtc),
   }),
   /** Rejects changes since snapshotAt or any explicit settled override to preserve user actions. */