diff --git a/src/auto-reply/get-reply-options.types.ts b/src/auto-reply/get-reply-options.types.ts
index a89b30a7079..ea74f01614f 100644
--- a/src/auto-reply/get-reply-options.types.ts
+++ b/src/auto-reply/get-reply-options.types.ts
@@ -1,3 +1,4 @@
+import type { AgentMessage } from "@earendil-works/pi-agent-core";
 import type { ImageContent } from "@earendil-works/pi-ai";
 import type { PromptImageOrderEntry } from "../media/prompt-image-order.js";
 import type { ReplyPayload } from "./reply-payload.js";
@@ -56,6 +57,10 @@ export type GetReplyOptions = {
   imageOrder?: PromptImageOrderEntry[];
   /** Notifies when an agent run actually starts (useful for webchat command handling). */
   onAgentRunStart?: (runId: string) => void;
+  /** Notifies when the runtime actually persists the current user turn. */
+  onUserMessagePersisted?: (
+    message: Extract<AgentMessage, { role: "user" }>,
+  ) => Promise<void> | void;
   onReplyStart?: () => Promise<void> | void;
   /** Called when the typing controller cleans up (e.g., run ended with NO_REPLY). */
   onTypingCleanup?: () => void;
diff --git a/src/auto-reply/reply/followup-runner.ts b/src/auto-reply/reply/followup-runner.ts
index 7521374ce74..92a31c02828 100644
--- a/src/auto-reply/reply/followup-runner.ts
+++ b/src/auto-reply/reply/followup-runner.ts
@@ -693,6 +693,12 @@ export function createFollowupRunner(params: {
                   }) ??
                   provider);
             let attemptCompactionCount = 0;
+            const notifyUserMessagePersisted = async (
+              message: Parameters<NonNullable<GetReplyOptions["onUserMessagePersisted"]>>[0],
+            ) => {
+              queuedUserMessagePersistedAcrossFallback = true;
+              await opts?.onUserMessagePersisted?.(message);
+            };
             try {
               if (isCliProvider(cliExecutionProvider, runtimeConfig)) {
                 const isRoomEventCliRun = queued.currentInboundEventKind === "room_event";
@@ -727,9 +733,7 @@ export function createFollowupRunner(params: {
                       ? { message: effectiveQueued.userMessageForPersistence }
                       : { text: effectiveQueued.transcriptPrompt ?? effectiveQueued.prompt },
                     suppressNextUserMessagePersistence: suppressQueuedUserPersistenceForCandidate,
-                    onUserMessagePersisted: () => {
-                      queuedUserMessagePersistedAcrossFallback = true;
-                    },
+                    onUserMessagePersisted: notifyUserMessagePersisted,
                     currentInboundEventKind: queued.currentInboundEventKind,
                     currentInboundContext: queued.currentInboundContext,
                     inputProvenance: run.inputProvenance,
@@ -828,9 +832,7 @@ export function createFollowupRunner(params: {
                 sourceReplyDeliveryMode: run.sourceReplyDeliveryMode,
                 forceMessageTool: run.sourceReplyDeliveryMode === "message_tool_only",
                 suppressNextUserMessagePersistence: suppressQueuedUserPersistenceForCandidate,
-                onUserMessagePersisted: () => {
-                  queuedUserMessagePersistedAcrossFallback = true;
-                },
+                onUserMessagePersisted: notifyUserMessagePersisted,
                 suppressTranscriptOnlyAssistantPersistence:
                   run.suppressTranscriptOnlyAssistantPersistence,
                 suppressAssistantErrorPersistence: suppressAssistantErrorPersistenceForCandidate,
diff --git a/src/gateway/server-methods/chat.directive-tags.test.ts b/src/gateway/server-methods/chat.directive-tags.test.ts
index ffebaa259f4..bc5e184e0e4 100644
--- a/src/gateway/server-methods/chat.directive-tags.test.ts
+++ b/src/gateway/server-methods/chat.directive-tags.test.ts
@@ -56,6 +56,7 @@ const mockState = vi.hoisted(() => ({
   dispatchError: null as Error | null,
   dispatchErrorAfterAgentRunStart: null as Error | null,
   triggerAgentRunStart: false,
+  triggerUserMessagePersisted: false,
   onAfterAgentRunStart: null as (() => void) | null,
   agentRunId: "run-agent-1",
   sessionEntry: {} as Record<string, unknown>,
@@ -192,6 +193,7 @@ vi.mock("../../auto-reply/dispatch.js", () => ({
       };
       replyOptions?: {
         onAgentRunStart?: (runId: string) => void;
+        onUserMessagePersisted?: (message: { role: "user"; content: string }) => void;
         images?: Array<{ mimeType: string; data: string }>;
         imageOrder?: string[];
       };
@@ -208,6 +210,12 @@ vi.mock("../../auto-reply/dispatch.js", () => ({
         params.replyOptions?.onAgentRunStart?.(mockState.agentRunId);
         mockState.onAfterAgentRunStart?.();
       }
+      if (mockState.triggerUserMessagePersisted) {
+        params.replyOptions?.onUserMessagePersisted?.({
+          role: "user",
+          content: "persisted by runtime",
+        });
+      }
       if (mockState.dispatchErrorAfterAgentRunStart) {
         throw mockState.dispatchErrorAfterAgentRunStart;
       }
@@ -700,6 +708,7 @@ describe("chat directive tag stripping for non-streaming final payloads", () =>
     mockState.dispatchErrorAfterAgentRunStart = null;
     mockState.mainSessionKey = "main";
     mockState.triggerAgentRunStart = false;
+    mockState.triggerUserMessagePersisted = false;
     mockState.onAfterAgentRunStart = null;
     mockState.agentRunId = "run-agent-1";
     mockState.sessionEntry = {};
@@ -4376,6 +4385,43 @@ describe("chat directive tag stripping for non-streaming final payloads", () =>
       expect(persistedUser?.content).toBe("hello from failed dispatch");
     });
   });
+
+  it("emits a user transcript update when chat.send fails after agent start but before runtime persistence", async () => {
+    createTranscriptFixture("openclaw-chat-send-user-transcript-error-before-runtime-persist-");
+    mockState.triggerAgentRunStart = true;
+    mockState.dispatchErrorAfterAgentRunStart = new Error("cli backend unavailable");
+    const respond = vi.fn();
+    const context = createChatContext();
+
+    await runNonStreamingChatSend({
+      context,
+      respond,
+      idempotencyKey: "idem-user-transcript-error-before-runtime-persist",
+      message: "hello before cli startup failure",
+      expectBroadcast: false,
+    });
+
+    await waitForAssertion(() => {
+      expect(context.dedupe.get("chat:idem-user-transcript-error-before-runtime-persist")?.ok).toBe(
+        false,
+      );
+      const userUpdate = findUserUpdate();
+      const message = userUpdateMessage(userUpdate);
+      expect(userUpdate?.sessionFile.endsWith("sess.jsonl")).toBe(true);
+      expect(userUpdate?.sessionKey).toBe("main");
+      expect(message?.role).toBe("user");
+      expect(message?.content).toBe("hello before cli startup failure");
+      const persistedUser = readTranscriptJsonLines(mockState.transcriptPath)
+        .map((entry) => entry.message)
+        .find(
+          (candidate): candidate is Record<string, unknown> =>
+            typeof candidate === "object" &&
+            candidate !== null &&
+            (candidate as { role?: unknown }).role === "user",
+        );
+      expect(persistedUser?.content).toBe("hello before cli startup failure");
+    });
+  });
 });
 
 describe("chat.send operator UI client sender context", () => {
diff --git a/src/gateway/server-methods/chat.ts b/src/gateway/server-methods/chat.ts
index 8a13b5965b0..9d1566feff4 100644
--- a/src/gateway/server-methods/chat.ts
+++ b/src/gateway/server-methods/chat.ts
@@ -48,6 +48,7 @@ import {
 import { createChannelMessageReplyPipeline } from "../../plugin-sdk/channel-message.js";
 import type { ChannelRouteRef } from "../../plugin-sdk/channel-route.js";
 import { isPluginOwnedSessionBindingRecord } from "../../plugins/conversation-binding.js";
+import { getGlobalHookRunner } from "../../plugins/hook-runner-global.js";
 import { normalizeInputProvenance, type InputProvenance } from "../../sessions/input-provenance.js";
 import { resolveSendPolicy } from "../../sessions/send-policy.js";
 import { parseAgentSessionKey } from "../../sessions/session-key-utils.js";
@@ -2676,6 +2677,9 @@ export const chatHandlers: GatewayRequestHandlers = {
       let appendedWebchatAgentMedia = false;
       let userTranscriptUpdatePromise: Promise<void> | null = null;
       let agentRunStarted = false;
+      let agentUserMessagePersisted = false;
+      const beforeAgentRunHooksRegistered =
+        getGlobalHookRunner()?.hasHooks("before_agent_run") === true;
       const persistGatewayUserTurnTranscript = async () => {
         if (userTranscriptUpdatePromise) {
           await userTranscriptUpdatePromise;
@@ -2870,6 +2874,9 @@ export const chatHandlers: GatewayRequestHandlers = {
                   }
                 }
               },
+              onUserMessagePersisted: () => {
+                agentUserMessagePersisted = true;
+              },
               onModelSelected: (modelSelection) => {
                 updateChatRunProvider(context.chatAbortControllers, {
                   runId: clientRunId,
@@ -3446,9 +3453,10 @@ export const chatHandlers: GatewayRequestHandlers = {
           );
         })
         .catch(async (err) => {
-          const emitAfterError = agentRunStarted
-            ? Promise.resolve()
-            : persistGatewayUserTurnTranscript();
+          const emitAfterError =
+            agentUserMessagePersisted || beforeAgentRunHooksRegistered
+              ? Promise.resolve()
+              : persistGatewayUserTurnTranscript();
           await emitAfterError.catch((transcriptErr) => {
             context.logGateway.warn(
               `webchat user transcript update failed after error: ${formatForLog(transcriptErr)}`,