diff --git a/src/agents/cli-auth-epoch.test.ts b/src/agents/cli-auth-epoch.test.ts
index 97be9acf190..62d0b411abd 100644
--- a/src/agents/cli-auth-epoch.test.ts
+++ b/src/agents/cli-auth-epoch.test.ts
@@ -47,6 +47,71 @@ describe("resolveCliAuthEpoch", () => {
     ).resolves.toBeUndefined();
   });
 
+  it("loads auth-profile epochs from the selected agent directory", async () => {
+    const stores: Record<string, AuthProfileStore> = {
+      "/agents/work/agent": {
+        version: 1,
+        profiles: {
+          "google-gemini-cli:default": {
+            type: "oauth",
+            provider: "google-gemini-cli",
+            access: "work-access",
+            refresh: "work-refresh",
+            expires: 1,
+            email: "work@example.test",
+            projectId: "work-project",
+          },
+        },
+      },
+      "/agents/personal/agent": {
+        version: 1,
+        profiles: {
+          "google-gemini-cli:default": {
+            type: "oauth",
+            provider: "google-gemini-cli",
+            access: "personal-access",
+            refresh: "personal-refresh",
+            expires: 1,
+            email: "personal@example.test",
+            projectId: "personal-project",
+          },
+        },
+      },
+    };
+    const loadAuthProfileStoreForRuntime = vi.fn((agentDir?: string) => {
+      return stores[agentDir ?? ""] ?? { version: 1, profiles: {} };
+    });
+    setCliAuthEpochTestDeps({
+      readGeminiCliCredentialsCached: () => null,
+      loadAuthProfileStoreForRuntime,
+    });
+
+    const work = await resolveCliAuthEpoch({
+      provider: "google-gemini-cli",
+      agentDir: "/agents/work/agent",
+      authProfileId: "google-gemini-cli:default",
+      skipLocalCredential: true,
+    });
+    const personal = await resolveCliAuthEpoch({
+      provider: "google-gemini-cli",
+      agentDir: "/agents/personal/agent",
+      authProfileId: "google-gemini-cli:default",
+      skipLocalCredential: true,
+    });
+
+    expectCliAuthEpoch(work);
+    expectCliAuthEpoch(personal);
+    expect(work).not.toBe(personal);
+    expect(loadAuthProfileStoreForRuntime).toHaveBeenCalledWith("/agents/work/agent", {
+      readOnly: true,
+      allowKeychainPrompt: false,
+    });
+    expect(loadAuthProfileStoreForRuntime).toHaveBeenCalledWith("/agents/personal/agent", {
+      readOnly: true,
+      allowKeychainPrompt: false,
+    });
+  });
+
   it("keeps identity-less claude cli oauth epochs stable across token changes", async () => {
     let access = "access-a";
     let refresh = "refresh-a";
diff --git a/src/agents/cli-auth-epoch.ts b/src/agents/cli-auth-epoch.ts
index 871e2be9e96..dfdac2d959f 100644
--- a/src/agents/cli-auth-epoch.ts
+++ b/src/agents/cli-auth-epoch.ts
@@ -208,6 +208,7 @@ function getAuthProfileCredential(
 /** Resolves the stable auth epoch hash for a CLI runtime/provider session. */
 export async function resolveCliAuthEpoch(params: {
   provider: string;
+  agentDir?: string;
   authProfileId?: string;
   skipLocalCredential?: boolean;
 }): Promise<string | undefined> {
@@ -223,7 +224,7 @@ export async function resolveCliAuthEpoch(params: {
   }
 
   if (authProfileId) {
-    const store = cliAuthEpochDeps.loadAuthProfileStoreForRuntime(undefined, {
+    const store = cliAuthEpochDeps.loadAuthProfileStoreForRuntime(params.agentDir, {
       readOnly: true,
       allowKeychainPrompt: false,
     });
diff --git a/src/agents/cli-runner/prepare.ts b/src/agents/cli-runner/prepare.ts
index 427633531eb..41870f3a80e 100644
--- a/src/agents/cli-runner/prepare.ts
+++ b/src/agents/cli-runner/prepare.ts
@@ -485,6 +485,7 @@ export async function prepareCliRunContext(
   });
   const authEpoch = await resolveCliAuthEpoch({
     provider: params.provider,
+    agentDir,
     authProfileId: effectiveAuthProfileId,
     skipLocalCredential: skipLocalCredentialEpoch,
   });