diff --git a/src/commands/run.ts b/src/commands/run.ts
index 050e3e3c6..2e9f5c8a3 100644
--- a/src/commands/run.ts
+++ b/src/commands/run.ts
@@ -328,7 +328,8 @@ export class RunCommand extends ApifyCommand<typeof RunCommand> {
 
 		if (proxy && proxy.password) localEnvVars[APIFY_ENV_VARS.PROXY_PASSWORD] = proxy.password;
 		if (userId) localEnvVars[APIFY_ENV_VARS.USER_ID] = userId;
-		if (token) localEnvVars[APIFY_ENV_VARS.TOKEN] = token;
+		// Don't clobber an explicitly-set APIFY_TOKEN inherited from the environment — it must win over the stored login.
+		if (token && !process.env[APIFY_ENV_VARS.TOKEN]) localEnvVars[APIFY_ENV_VARS.TOKEN] = token;
 		if (localConfig!.environmentVariables) {
 			const updatedEnv = replaceSecretsValue(localConfig!.environmentVariables as Record<string, string>, undefined, {
 				allowMissing: this.flags.allowMissingSecrets,
diff --git a/src/lib/utils.ts b/src/lib/utils.ts
index 99d8784e8..ae00a50b1 100644
--- a/src/lib/utils.ts
+++ b/src/lib/utils.ts
@@ -131,6 +131,7 @@ export async function getLoggedClientOrThrow() {
 
 const resolveToken = async (existingToken?: string): Promise<string | undefined> => {
 	if (existingToken) return existingToken;
+	if (process.env[APIFY_ENV_VARS.TOKEN]) return process.env[APIFY_ENV_VARS.TOKEN];
 	await ensureMigrated();
 	return getToken();
 };
diff --git a/test/local/commands/run.test.ts b/test/local/commands/run.test.ts
index bc4e26323..bd438ab92 100644
--- a/test/local/commands/run.test.ts
+++ b/test/local/commands/run.test.ts
@@ -216,6 +216,33 @@ describe('apify run', () => {
 		expect(actOutput2).toStrictEqual('can play');
 	});
 
+	// Regression: an inherited APIFY_TOKEN must reach the Actor unchanged, not be clobbered by the stored login token.
+	it(`[api] does not override an inherited ${APIFY_ENV_VARS.TOKEN} with the stored token`, async () => {
+		await safeLogin();
+
+		const auth = JSON.parse(readFileSync(AUTH_FILE_PATH(), 'utf8'));
+		const inheritedToken = `${auth.token}_inherited`;
+		vitest.stubEnv(APIFY_ENV_VARS.TOKEN, inheritedToken);
+
+		const actCode = `
+        import { Actor } from 'apify';
+
+        Actor.main(async () => {
+            await Actor.setValue('OUTPUT', process.env);
+            console.log('Done.');
+        });
+        `;
+		writeFileSync(joinPath('src/main.js'), actCode, { flag: 'w' });
+
+		await testRunCommand(RunCommand, {});
+
+		const actOutputPath = joinPath(getLocalKeyValueStorePath(), 'OUTPUT.json');
+		const localEnvVars = JSON.parse(readFileSync(actOutputPath, 'utf8'));
+
+		expect(localEnvVars[APIFY_ENV_VARS.TOKEN]).toStrictEqual(inheritedToken);
+		expect(localEnvVars[APIFY_ENV_VARS.TOKEN]).not.toStrictEqual(auth.token);
+	});
+
 	it('run purge stores', async () => {
 		const input = {
 			myInput: 'value',
diff --git a/test/local/lib/credentials.test.ts b/test/local/lib/credentials.test.ts
index 4a0566ed8..4b78727fa 100644
--- a/test/local/lib/credentials.test.ts
+++ b/test/local/lib/credentials.test.ts
@@ -14,7 +14,7 @@ import {
 	setProxyPassword,
 	setToken,
 } from '../../../src/lib/credentials.js';
-import { getLocalUserInfo } from '../../../src/lib/utils.js';
+import { getApifyClientOptions, getLocalUserInfo } from '../../../src/lib/utils.js';
 
 const keyringStore = new Map<string, string>();
 const keyringFailures = new Set<string>();
@@ -278,4 +278,30 @@ describe('credentials', () => {
 			expect(info.proxy?.password).toBe('pw_kr');
 		});
 	});
+
+	// Precedence: explicit token arg (e.g. --token) > APIFY_TOKEN env var > stored login token.
+	// Regression guard for the env var being ignored in favour of the stored token.
+	describe('token resolution precedence (getApifyClientOptions)', () => {
+		it('prefers the APIFY_TOKEN env var over the stored token', async () => {
+			vitest.stubEnv('APIFY_DISABLE_KEYRING', '1');
+			await setToken('stored_tok');
+			vitest.stubEnv('APIFY_TOKEN', 'env_tok');
+			const { token } = await getApifyClientOptions();
+			expect(token).toBe('env_tok');
+		});
+
+		it('prefers an explicitly passed token over the APIFY_TOKEN env var', async () => {
+			vitest.stubEnv('APIFY_TOKEN', 'env_tok');
+			const { token } = await getApifyClientOptions('explicit_tok');
+			expect(token).toBe('explicit_tok');
+		});
+
+		it('falls back to the stored token when APIFY_TOKEN is not set', async () => {
+			vitest.stubEnv('APIFY_DISABLE_KEYRING', '1');
+			vitest.stubEnv('APIFY_TOKEN', '');
+			await setToken('stored_tok');
+			const { token } = await getApifyClientOptions();
+			expect(token).toBe('stored_tok');
+		});
+	});
 });