diff --git a/packages/agent/src/adapters/local-tools/tools/list-repos.ts b/packages/agent/src/adapters/local-tools/tools/list-repos.ts
index d11287a64b..5432a49c8d 100644
--- a/packages/agent/src/adapters/local-tools/tools/list-repos.ts
+++ b/packages/agent/src/adapters/local-tools/tools/list-repos.ts
@@ -60,8 +60,16 @@ export const listReposTool = defineLocalTool({
     );
 
     try {
+      // An empty token is a managed logout, not "no preference": clear both token
+      // vars so gh cannot fall back to the previous actor's frozen process-env
+      // token and enumerate their private repos. Only an undefined token (an
+      // unmanaged local/desktop sandbox) inherits the process env unchanged.
+      const env =
+        token === undefined
+          ? process.env
+          : { ...process.env, GH_TOKEN: token, GITHUB_TOKEN: token };
       const { stdout } = await execFileAsync("gh", cmdArgs, {
-        env: token ? { ...process.env, GH_TOKEN: token } : process.env,
+        env,
         maxBuffer: 1024 * 1024 * 8,
       });
       const parsed = ghRepoSchema.safeParse(JSON.parse(stdout));
diff --git a/packages/agent/src/server/agent-server.ts b/packages/agent/src/server/agent-server.ts
index 224f42fa16..0b980a6b4a 100644
--- a/packages/agent/src/server/agent-server.ts
+++ b/packages/agent/src/server/agent-server.ts
@@ -16,6 +16,7 @@ import {
 import { type ServerType, serve } from "@hono/node-server";
 import { execGh } from "@posthog/git/gh";
 import { getCurrentBranch } from "@posthog/git/queries";
+import { ghTokenEnv } from "@posthog/git/signed-commit";
 import {
   type Adapter,
   buildPrOutput,
@@ -94,6 +95,7 @@ import {
   resolveGatewayProduct,
   resolveLlmGatewayUrl,
 } from "../utils/gateway";
+import { resolveGithubToken } from "../utils/github-token";
 import { Logger } from "../utils/logger";
 import { logAgentshRuntimeInfo } from "./agentsh-runtime";
 import {
@@ -4405,6 +4407,15 @@ ${signedCommitInstructions}${prLinkInstructions}${shellEfficiencyInstructions}
     }
   }
 
+  /** Env for a `gh` call that must run as the *current* actor. Prefers the live
+   *  sandbox token (rewritten on an actor transition) over the process env
+   *  (frozen at launch); returns undefined when unmanaged (local/desktop) so
+   *  execGh falls back to the process env. */
+  private ghActorEnv(): Record<string, string> | undefined {
+    const token = resolveGithubToken();
+    return token === undefined ? undefined : ghTokenEnv(token);
+  }
+
   private async fetchPrAttribution(
     prUrl: string,
   ): Promise<{ createdAt: string | null; author: string | null }> {
@@ -4413,6 +4424,7 @@ ${signedCommitInstructions}${prLinkInstructions}${shellEfficiencyInstructions}
       {
         cwd: this.config.repositoryPath,
         timeoutMs: 10_000,
+        env: this.ghActorEnv(),
       },
     );
     if (res.exitCode !== 0) return { createdAt: null, author: null };
@@ -4431,11 +4443,21 @@ ${signedCommitInstructions}${prLinkInstructions}${shellEfficiencyInstructions}
   }
 
   private ghLoginPromise: Promise<string | null> | null = null;
+  private ghLoginToken: string | undefined;
 
   private fetchGhLogin(): Promise<string | null> {
-    this.ghLoginPromise ??= execGh(["api", "user", "--jq", ".login"], {
+    // Key the memoized login on the live token: an actor transition rebinds
+    // /tmp/agent-env, so a cached login would otherwise attribute the new actor's
+    // work to the previous one (or reject their PR).
+    const token = resolveGithubToken();
+    if (this.ghLoginPromise !== null && this.ghLoginToken === token) {
+      return this.ghLoginPromise;
+    }
+    this.ghLoginToken = token;
+    this.ghLoginPromise = execGh(["api", "user", "--jq", ".login"], {
       cwd: this.config.repositoryPath,
       timeoutMs: 10_000,
+      env: token === undefined ? undefined : ghTokenEnv(token),
     })
       .then((res) => {
         const login = res.exitCode === 0 ? res.stdout.trim() : "";
diff --git a/packages/agent/src/utils/github-token.test.ts b/packages/agent/src/utils/github-token.test.ts
index 08ef9428b9..3b1dccd254 100644
--- a/packages/agent/src/utils/github-token.test.ts
+++ b/packages/agent/src/utils/github-token.test.ts
@@ -49,10 +49,33 @@ describe("github-token", () => {
       ).toBeUndefined();
     });
 
+    it("fails closed ('') when the file exists but is unreadable (not ENOENT)", () => {
+      // A directory path triggers EISDIR, standing in for a transiently unreadable
+      // managed file during a transition — must not resurrect the process env.
+      const dir = mkdtempSync(join(tmpdir(), "agent-env-dir-"));
+      expect(readGithubTokenFromSandboxEnvFile(dir)).toBe("");
+    });
+
     it("ignores an empty token value", () => {
       const path = writeEnvFile("GH_TOKEN=\0GITHUB_TOKEN=ghs_real\0");
       expect(readGithubTokenFromSandboxEnvFile(path)).toBe("ghs_real");
     });
+
+    it("returns '' (explicit logout) when every token var is present but empty", () => {
+      const path = writeEnvFile("PATH=/usr/bin\0GH_TOKEN=\0GITHUB_TOKEN=\0");
+      expect(readGithubTokenFromSandboxEnvFile(path)).toBe("");
+    });
+
+    it("returns '' (logout) when the managed file is truncated to zero bytes", () => {
+      // The backend logs the sandbox out by writing an empty file, not emptied vars.
+      expect(readGithubTokenFromSandboxEnvFile(writeEnvFile(""))).toBe("");
+      expect(readGithubTokenFromSandboxEnvFile(writeEnvFile("   \n"))).toBe("");
+    });
+
+    it("returns undefined when the file carries no token var at all", () => {
+      const path = writeEnvFile("PATH=/usr/bin\0HOME=/root\0");
+      expect(readGithubTokenFromSandboxEnvFile(path)).toBeUndefined();
+    });
   });
 
   describe("resolveGithubToken", () => {
@@ -72,5 +95,35 @@ describe("github-token", () => {
         "ghs_fromprocess",
       );
     });
+
+    it("does not resurrect the process-env token after a logout (emptied file)", () => {
+      // The backend logs the sandbox out by emptying the token vars in the file.
+      // The frozen launch-time process env still holds the previous actor's
+      // token; resolving must NOT fall back to it.
+      vi.stubEnv("GH_TOKEN", "ghs_previous_actor");
+      const path = writeEnvFile("GH_TOKEN=\0GITHUB_TOKEN=\0");
+      expect(resolveGithubToken(path)).toBe("");
+    });
+
+    it("does not resurrect the process-env token when the file is zero bytes (logout)", () => {
+      // The backend's actual logout truncates the file to zero bytes; resolving
+      // must treat that as logout, not fall back to the frozen process env.
+      vi.stubEnv("GH_TOKEN", "ghs_previous_actor");
+      expect(resolveGithubToken(writeEnvFile(""))).toBe("");
+    });
+
+    it("falls back to the process env when the file carries no token var", () => {
+      vi.stubEnv("GH_TOKEN", "ghs_fromprocess");
+      const path = writeEnvFile("PATH=/usr/bin\0");
+      expect(resolveGithubToken(path)).toBe("ghs_fromprocess");
+    });
+
+    it("does not fall back to the process env when the file is unreadable", () => {
+      // Present-but-unreadable (EISDIR here) is a managed sandbox mid-transition,
+      // not an absent file, so it must not resurrect the frozen process token.
+      vi.stubEnv("GH_TOKEN", "ghs_previous_actor");
+      const dir = mkdtempSync(join(tmpdir(), "agent-env-dir-"));
+      expect(resolveGithubToken(dir)).toBe("");
+    });
   });
 });
diff --git a/packages/agent/src/utils/github-token.ts b/packages/agent/src/utils/github-token.ts
index 1e1ae73228..5486cc9d48 100644
--- a/packages/agent/src/utils/github-token.ts
+++ b/packages/agent/src/utils/github-token.ts
@@ -1,5 +1,8 @@
 import { readFileSync } from "node:fs";
-import { readGithubTokenFromEnv } from "@posthog/git/signed-commit";
+import {
+  GITHUB_TOKEN_ENV_VARS,
+  readGithubTokenFromEnv,
+} from "@posthog/git/signed-commit";
 
 // helpers for resolving the in-sandbox GitHub token
 // Dedicated agentsh credential file (NUL-delimited `key=value` pairs) that the
@@ -12,19 +15,45 @@ const SANDBOX_GITHUB_ENV_FILE = "/tmp/agent-github-env";
 export function readGithubTokenFromSandboxEnvFile(
   envFilePath: string = SANDBOX_GITHUB_ENV_FILE,
 ): string | undefined {
+  let raw: string;
   try {
-    const raw = readFileSync(envFilePath, "utf8");
-    const env: Record<string, string> = {};
-    for (const entry of raw.split("\0")) {
-      const eq = entry.indexOf("=");
-      if (eq > 0) {
-        env[entry.slice(0, eq)] = entry.slice(eq + 1);
-      }
+    raw = readFileSync(envFilePath, "utf8");
+  } catch (err) {
+    // A genuinely absent file (local/desktop or test) is unmanaged: signal that so
+    // the caller falls back to the process env. But an existing-yet-unreadable file
+    // during an actor transition must NOT resurrect the frozen process token, so
+    // treat any other read error as an explicit logout (fail closed).
+    if ((err as NodeJS.ErrnoException).code === "ENOENT") {
+      return undefined;
     }
-    // Reuse the shared token-var allowlist + precedence instead of hardcoding.
-    return readGithubTokenFromEnv(env);
-  } catch {
-    // No env file (local/desktop or test) — fall back to the process env.
+    return "";
+  }
+  // The backend logs the sandbox out by truncating this file to zero bytes, so a
+  // successfully-read but empty (or whitespace-only) managed file is an explicit
+  // logout — return "" so the caller does NOT resurrect the previous actor's token
+  // from the frozen launch-time process env. Only an absent file is "unmanaged".
+  if (raw.trim() === "") {
+    return "";
+  }
+  const env: Record<string, string> = {};
+  for (const entry of raw.split("\0")) {
+    const eq = entry.indexOf("=");
+    if (eq > 0) {
+      env[entry.slice(0, eq)] = entry.slice(eq + 1);
+    }
+  }
+  // A non-empty value wins by the shared token-var precedence.
+  const token = readGithubTokenFromEnv(env);
+  if (token) {
+    return token;
+  }
+  // The file is the backend's live credential channel. If it carries the token
+  // vars but they are emptied, that is an explicit logout on an actor
+  // transition — return "" so the caller does NOT resurrect the previous
+  // actor's token from the frozen launch-time process env. Only a file with no
+  // token vars at all is "unmanaged" and defers to the process env.
+  if (GITHUB_TOKEN_ENV_VARS.some((name) => name in env)) {
+    return "";
   }
   return undefined;
 }