diff --git a/extensions/matrix/src/matrix/monitor/handler.test-helpers.ts b/extensions/matrix/src/matrix/monitor/handler.test-helpers.ts
index 3aa13a735a0..4344e4a0d61 100644
--- a/extensions/matrix/src/matrix/monitor/handler.test-helpers.ts
+++ b/extensions/matrix/src/matrix/monitor/handler.test-helpers.ts
@@ -27,6 +27,7 @@ type MatrixHandlerTestHarnessOptions = {
   accountAllowBots?: boolean | "mentions";
   configuredBotUserIds?: Set<string>;
   mentionRegexes?: MatrixMonitorHandlerParams["mentionRegexes"];
+  buildMentionRegexes?: MatrixMonitorHandlerParams["core"]["channel"]["mentions"]["buildMentionRegexes"];
   groupPolicy?: "open" | "allowlist" | "disabled";
   replyToMode?: ReplyToMode;
   threadReplies?: "off" | "inbound" | "always";
@@ -142,6 +143,9 @@ export function createMatrixHandlerTestHarness(
           resolveHumanDelayConfig: options.resolveHumanDelayConfig ?? (() => undefined),
           dispatchReplyFromConfig,
         },
+        mentions: {
+          buildMentionRegexes: options.buildMentionRegexes ?? (() => []),
+        },
         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 289623631fa..d3cf39c4056 100644
--- a/extensions/matrix/src/matrix/monitor/handler.test.ts
+++ b/extensions/matrix/src/matrix/monitor/handler.test.ts
@@ -426,8 +426,8 @@ describe("matrix monitor handler pairing account scope", () => {
     expect(recordInboundSession).not.toHaveBeenCalled();
   });
 
-  it("drops forged metadata-only mentions before agent routing", async () => {
-    const { handler, recordInboundSession, resolveAgentRoute } = createMatrixHandlerTestHarness({
+  it("drops forged metadata-only mentions without processing", async () => {
+    const { handler, recordInboundSession } = createMatrixHandlerTestHarness({
       isDirectMessage: false,
       mentionRegexes: [/@bot/i],
       getMemberDisplayName: async () => "sender",
@@ -442,7 +442,6 @@ describe("matrix monitor handler pairing account scope", () => {
       }),
     );
 
-    expect(resolveAgentRoute).not.toHaveBeenCalled();
     expect(recordInboundSession).not.toHaveBeenCalled();
   });
 
@@ -477,9 +476,6 @@ describe("matrix monitor handler pairing account scope", () => {
     } as MatrixRawEvent);
 
     expect(downloadContent).not.toHaveBeenCalled();
-    expect(getMemberDisplayName).not.toHaveBeenCalled();
-    expect(getRoomInfo).not.toHaveBeenCalled();
-    expect(resolveAgentRoute).not.toHaveBeenCalled();
   });
 
   it("skips poll snapshot fetches for unmentioned group poll responses", async () => {
@@ -988,4 +984,36 @@ describe("matrix monitor handler pairing account scope", () => {
 
     expect(resolveAgentRoute).toHaveBeenCalledTimes(1);
   });
+
+  it("re-resolves mentions with agent-level patterns after route resolution (#51082)", async () => {
+    const buildMentionRegexes = vi.fn((_cfg: unknown, agentId?: string) => {
+      if (!agentId) return [];
+      return [/@mybot/i];
+    });
+    const dispatchReplyFromConfig = vi.fn(async () => ({
+      queuedFinal: false,
+      counts: { final: 0, block: 0, tool: 0 },
+    }));
+    const { handler } = createMatrixHandlerTestHarness({
+      mentionRegexes: [],
+      buildMentionRegexes,
+      roomsConfig: {
+        "!room:example.org": { requireMention: true },
+      },
+      isDirectMessage: false,
+      groupPolicy: "open",
+      dispatchReplyFromConfig,
+    });
+
+    await handler(
+      "!room:example.org",
+      createMatrixTextMessageEvent({
+        eventId: "$agent-mention",
+        body: "hey @mybot can you help?",
+      }),
+    );
+
+    expect(buildMentionRegexes).toHaveBeenCalledWith(expect.anything(), "ops");
+    expect(dispatchReplyFromConfig).toHaveBeenCalled();
+  });
 });
diff --git a/extensions/matrix/src/matrix/monitor/handler.ts b/extensions/matrix/src/matrix/monitor/handler.ts
index b7295009bcd..b6388654cfd 100644
--- a/extensions/matrix/src/matrix/monitor/handler.ts
+++ b/extensions/matrix/src/matrix/monitor/handler.ts
@@ -494,7 +494,7 @@ export function createMatrixRoomMessageHandler(params: MatrixMonitorHandlerParam
         return;
       }
 
-      const { wasMentioned, hasExplicitMention } = resolveMentions({
+      let { wasMentioned, hasExplicitMention } = resolveMentions({
         content,
         userId: selfUserId,
         text: mentionPrecheckText,
@@ -554,10 +554,21 @@ export function createMatrixRoomMessageHandler(params: MatrixMonitorHandlerParam
         commandAuthorized &&
         hasControlCommandInMessage;
       const canDetectMention = mentionRegexes.length > 0 || hasExplicitMention;
-      if (isRoom && shouldRequireMention && !wasMentioned && !shouldBypassMention) {
+      // When there is message text, defer mention drop until after route
+      // resolution so agent-level mentionPatterns are checked (#51082).
+      // Media-only/poll events have no text - drop them immediately.
+      if (
+        isRoom &&
+        shouldRequireMention &&
+        !wasMentioned &&
+        !shouldBypassMention &&
+        !mentionPrecheckText
+      ) {
         logger.info("skipping room message", { roomId, reason: "no-mention" });
         return;
       }
+      const mentionDropDeferred =
+        isRoom && shouldRequireMention && !wasMentioned && !shouldBypassMention;
 
       if (isPollEvent) {
         const pollSnapshot = await fetchMatrixPollSnapshot(client, roomId, event).catch((err) => {
@@ -661,6 +672,28 @@ export function createMatrixRoomMessageHandler(params: MatrixMonitorHandlerParam
         eventTs: eventTs ?? undefined,
         resolveAgentRoute: core.channel.routing.resolveAgentRoute,
       });
+
+      // Re-resolve mentions with agent-specific mentionPatterns now that the
+      // route (and agentId) is known (#51082).
+      if (mentionDropDeferred) {
+        const agentMentionRegexes = core.channel.mentions.buildMentionRegexes(cfg, route.agentId);
+        if (agentMentionRegexes.length > 0) {
+          const agentMentionResult = resolveMentions({
+            content,
+            userId: selfUserId,
+            text: mentionPrecheckText,
+            mentionRegexes: agentMentionRegexes,
+          });
+          if (agentMentionResult.wasMentioned) {
+            wasMentioned = true;
+          }
+        }
+        if (!wasMentioned) {
+          logger.info("skipping room message", { roomId, reason: "no-mention" });
+          return;
+        }
+      }
+
       if (configuredBinding) {
         const ensured = await ensureConfiguredAcpBindingReady({
           cfg,