diff --git a/extensions/matrix/src/matrix/monitor/handler.test-helpers.ts b/extensions/matrix/src/matrix/monitor/handler.test-helpers.ts
index a6ddf28c110..4d17e8d42d0 100644
--- a/extensions/matrix/src/matrix/monitor/handler.test-helpers.ts
+++ b/extensions/matrix/src/matrix/monitor/handler.test-helpers.ts
@@ -56,12 +56,21 @@ type MatrixHandlerTestHarnessOptions = {
     dispatcher: Record<string, unknown>;
     replyOptions: Record<string, unknown>;
     markDispatchIdle: () => void;
+    markRunComplete: () => void;
   };
   resolveHumanDelayConfig?: () => undefined;
   dispatchReplyFromConfig?: () => Promise<{
     queuedFinal: boolean;
     counts: { final: number; block: number; tool: number };
   }>;
+  withReplyDispatcher?: <T>(params: {
+    dispatcher: {
+      markComplete?: () => void;
+      waitForIdle?: () => Promise<void>;
+    };
+    run: () => Promise<T>;
+    onSettled?: () => void | Promise<void>;
+  }) => Promise<T>;
   inboundDeduper?: MatrixMonitorHandlerParams["inboundDeduper"];
   shouldAckReaction?: () => boolean;
   enqueueSystemEvent?: (...args: unknown[]) => void;
@@ -139,9 +148,32 @@ export function createMatrixHandlerTestHarness(
               dispatcher: {},
               replyOptions: {},
               markDispatchIdle: () => {},
+              markRunComplete: () => {},
             })),
           resolveHumanDelayConfig: options.resolveHumanDelayConfig ?? (() => undefined),
           dispatchReplyFromConfig,
+          withReplyDispatcher:
+            options.withReplyDispatcher ??
+            (async <T>(params: {
+              dispatcher: {
+                markComplete?: () => void;
+                waitForIdle?: () => Promise<void>;
+              };
+              run: () => Promise<T>;
+              onSettled?: () => void | Promise<void>;
+            }) => {
+              const { dispatcher, run, onSettled } = params;
+              try {
+                return await run();
+              } finally {
+                dispatcher.markComplete?.();
+                try {
+                  await dispatcher.waitForIdle?.();
+                } finally {
+                  await onSettled?.();
+                }
+              }
+            }),
         },
         reactions: {
           shouldAckReaction: options.shouldAckReaction ?? (() => false),
diff --git a/extensions/matrix/src/matrix/monitor/handler.test.ts b/extensions/matrix/src/matrix/monitor/handler.test.ts
index 1f96e364ecc..19434083cf5 100644
--- a/extensions/matrix/src/matrix/monitor/handler.test.ts
+++ b/extensions/matrix/src/matrix/monitor/handler.test.ts
@@ -720,12 +720,36 @@ describe("matrix monitor handler pairing account scope", () => {
               dispatcher: {},
               replyOptions: {},
               markDispatchIdle: () => {},
+              markRunComplete: () => {},
             }),
             resolveHumanDelayConfig: () => undefined,
             dispatchReplyFromConfig: async () => ({
               queuedFinal: true,
               counts: { final: 1, block: 0, tool: 0 },
             }),
+            withReplyDispatcher: async <T>({
+              dispatcher,
+              run,
+              onSettled,
+            }: {
+              dispatcher: {
+                markComplete?: () => void;
+                waitForIdle?: () => Promise<void>;
+              };
+              run: () => Promise<T>;
+              onSettled?: () => void | Promise<void>;
+            }) => {
+              try {
+                return await run();
+              } finally {
+                dispatcher.markComplete?.();
+                try {
+                  await dispatcher.waitForIdle?.();
+                } finally {
+                  await onSettled?.();
+                }
+              }
+            },
           },
           reactions: {
             shouldAckReaction: () => false,
@@ -1022,7 +1046,7 @@ describe("matrix monitor handler durable inbound dedupe", () => {
     expect(inboundDeduper.releaseEvent).not.toHaveBeenCalled();
   });
 
-  it("commits inbound events before reply side effects", async () => {
+  it("commits inbound events only after queued replies finish delivering", async () => {
     const callOrder: string[] = [];
     const inboundDeduper = {
       claimEvent: vi.fn(() => {
@@ -1050,6 +1074,23 @@ describe("matrix monitor handler durable inbound dedupe", () => {
       inboundDeduper,
       recordInboundSession,
       dispatchReplyFromConfig,
+      createReplyDispatcherWithTyping: () => ({
+        dispatcher: {
+          markComplete: () => {
+            callOrder.push("mark-complete");
+          },
+          waitForIdle: async () => {
+            callOrder.push("wait-for-idle");
+          },
+        },
+        replyOptions: {},
+        markDispatchIdle: () => {
+          callOrder.push("dispatch-idle");
+        },
+        markRunComplete: () => {
+          callOrder.push("run-complete");
+        },
+      }),
     });
 
     await handler(
@@ -1060,7 +1101,16 @@ describe("matrix monitor handler durable inbound dedupe", () => {
       }),
     );
 
-    expect(callOrder).toEqual(["claim", "record", "dispatch", "commit"]);
+    expect(callOrder).toEqual([
+      "claim",
+      "record",
+      "dispatch",
+      "run-complete",
+      "mark-complete",
+      "wait-for-idle",
+      "dispatch-idle",
+      "commit",
+    ]);
     expect(inboundDeduper.releaseEvent).not.toHaveBeenCalled();
   });
 
diff --git a/extensions/matrix/src/matrix/monitor/handler.ts b/extensions/matrix/src/matrix/monitor/handler.ts
index 865c20d5a6a..8e34b04cec2 100644
--- a/extensions/matrix/src/matrix/monitor/handler.ts
+++ b/extensions/matrix/src/matrix/monitor/handler.ts
@@ -30,6 +30,7 @@ import {
 } from "../send.js";
 import { resolveMatrixMonitorAccessState } from "./access-state.js";
 import { resolveMatrixAckReactionConfig } from "./ack-config.js";
+import type { MatrixInboundEventDeduper } from "./inbound-dedupe.js";
 import { resolveMatrixLocation, type MatrixLocationPayload } from "./location.js";
 import { downloadMatrixMedia } from "./media.js";
 import { resolveMentions } from "./mentions.js";
@@ -72,11 +73,7 @@ export type MatrixMonitorHandlerParams = {
   startupMs: number;
   startupGraceMs: number;
   dropPreStartupMessages: boolean;
-  inboundDeduper?: {
-    claimEvent: (params: { roomId: string; eventId: string }) => boolean;
-    commitEvent: (params: { roomId: string; eventId: string; eventTs?: number }) => Promise<void>;
-    releaseEvent: (params: { roomId: string; eventId: string }) => void;
-  };
+  inboundDeduper?: Pick<MatrixInboundEventDeduper, "claimEvent" | "commitEvent" | "releaseEvent">;
   directTracker: {
     isDirectMessage: (params: {
       roomId: string;
@@ -268,11 +265,7 @@ export function createMatrixRoomMessageHandler(params: MatrixMonitorHandlerParam
         if (!claimedInboundEvent || !inboundDeduper || !eventId) {
           return;
         }
-        await inboundDeduper.commitEvent({
-          roomId,
-          eventId,
-          eventTs: eventTs ?? undefined,
-        });
+        await inboundDeduper.commitEvent({ roomId, eventId });
         claimedInboundEvent = false;
       };
       if (dropPreStartupMessages) {
@@ -871,7 +864,7 @@ export function createMatrixRoomMessageHandler(params: MatrixMonitorHandlerParam
           });
         },
       });
-      const { dispatcher, replyOptions, markDispatchIdle } =
+      const { dispatcher, replyOptions, markDispatchIdle, markRunComplete } =
         core.channel.reply.createReplyDispatcherWithTyping({
           ...prefixOptions,
           humanDelay: core.channel.reply.resolveHumanDelayConfig(cfg, route.agentId),
@@ -897,17 +890,28 @@ export function createMatrixRoomMessageHandler(params: MatrixMonitorHandlerParam
           onIdle: typingCallbacks.onIdle,
         });
 
-      const { queuedFinal, counts } = await core.channel.reply.dispatchReplyFromConfig({
-        ctx: ctxPayload,
-        cfg,
+      const { queuedFinal, counts } = await core.channel.reply.withReplyDispatcher({
         dispatcher,
-        replyOptions: {
-          ...replyOptions,
-          skillFilter: roomConfig?.skills,
-          onModelSelected,
+        onSettled: () => {
+          markDispatchIdle();
+        },
+        run: async () => {
+          try {
+            return await core.channel.reply.dispatchReplyFromConfig({
+              ctx: ctxPayload,
+              cfg,
+              dispatcher,
+              replyOptions: {
+                ...replyOptions,
+                skillFilter: roomConfig?.skills,
+                onModelSelected,
+              },
+            });
+          } finally {
+            markRunComplete();
+          }
         },
       });
-      markDispatchIdle();
       if (!queuedFinal) {
         await commitInboundEventIfClaimed();
         return;
diff --git a/extensions/matrix/src/matrix/monitor/inbound-dedupe.test.ts b/extensions/matrix/src/matrix/monitor/inbound-dedupe.test.ts
index da32ef4da66..e0ad423c1f1 100644
--- a/extensions/matrix/src/matrix/monitor/inbound-dedupe.test.ts
+++ b/extensions/matrix/src/matrix/monitor/inbound-dedupe.test.ts
@@ -97,4 +97,50 @@ describe("Matrix inbound event dedupe", () => {
     expect(deduper.claimEvent({ roomId: "!room:example.org", eventId: "$keep-2" })).toBe(false);
     expect(deduper.claimEvent({ roomId: "!room:example.org", eventId: "$keep-3" })).toBe(false);
   });
+
+  it("retains replayed backlog events based on processing time", async () => {
+    const storagePath = createStoragePath();
+    let now = 100;
+    const first = await createMatrixInboundEventDeduper({
+      auth: auth as never,
+      storagePath,
+      ttlMs: 20,
+      nowMs: () => now,
+    });
+
+    expect(first.claimEvent({ roomId: "!room:example.org", eventId: "$backlog" })).toBe(true);
+    await first.commitEvent({
+      roomId: "!room:example.org",
+      eventId: "$backlog",
+    });
+    await first.stop();
+
+    now = 110;
+    const second = await createMatrixInboundEventDeduper({
+      auth: auth as never,
+      storagePath,
+      ttlMs: 20,
+      nowMs: () => now,
+    });
+    expect(second.claimEvent({ roomId: "!room:example.org", eventId: "$backlog" })).toBe(false);
+  });
+
+  it("treats stop persistence failures as best-effort cleanup", async () => {
+    const blockingPath = createStoragePath();
+    fs.writeFileSync(blockingPath, "blocking file", "utf8");
+    const deduper = await createMatrixInboundEventDeduper({
+      auth: auth as never,
+      storagePath: path.join(blockingPath, "nested", "inbound-dedupe.json"),
+    });
+
+    expect(deduper.claimEvent({ roomId: "!room:example.org", eventId: "$persist-fail" })).toBe(
+      true,
+    );
+    await deduper.commitEvent({
+      roomId: "!room:example.org",
+      eventId: "$persist-fail",
+    });
+
+    await expect(deduper.stop()).resolves.toBeUndefined();
+  });
 });
diff --git a/extensions/matrix/src/matrix/monitor/inbound-dedupe.ts b/extensions/matrix/src/matrix/monitor/inbound-dedupe.ts
index e7ffa78af48..5784c1393a3 100644
--- a/extensions/matrix/src/matrix/monitor/inbound-dedupe.ts
+++ b/extensions/matrix/src/matrix/monitor/inbound-dedupe.ts
@@ -23,7 +23,7 @@ type StoredMatrixInboundDedupeState = {
 
 export type MatrixInboundEventDeduper = {
   claimEvent: (params: { roomId: string; eventId: string }) => boolean;
-  commitEvent: (params: { roomId: string; eventId: string; eventTs?: number }) => Promise<void>;
+  commitEvent: (params: { roomId: string; eventId: string }) => Promise<void>;
   releaseEvent: (params: { roomId: string; eventId: string }) => void;
   flush: () => Promise<void>;
   stop: () => Promise<void>;
@@ -252,13 +252,13 @@ export async function createMatrixInboundEventDeduper(params: {
       pending.add(key);
       return true;
     },
-    commitEvent: async ({ roomId, eventId, eventTs }) => {
+    commitEvent: async ({ roomId, eventId }) => {
       const key = buildEventKey({ roomId, eventId });
       if (!key) {
         return;
       }
       pending.delete(key);
-      const ts = normalizeTimestamp(eventTs) ?? nowMs();
+      const ts = nowMs();
       seen.delete(key);
       seen.set(key, ts);
       pruneSeenEvents({ seen, ttlMs, maxEntries, nowMs: nowMs() });
@@ -273,7 +273,15 @@ export async function createMatrixInboundEventDeduper(params: {
     },
     flush,
     stop: async () => {
-      await flush();
+      try {
+        await flush();
+      } catch (err) {
+        LogService.warn(
+          "MatrixInboundDedupe",
+          "Failed to flush Matrix inbound dedupe store during stop():",
+          err,
+        );
+      }
     },
   };
 }