diff --git a/app/Exceptions/Handler.php b/app/Exceptions/Handler.php
index 4b4df4971..c3a52ea35 100644
--- a/app/Exceptions/Handler.php
+++ b/app/Exceptions/Handler.php
@@ -4,9 +4,11 @@
 
 use App\Models\InstanceSettings;
 use App\Models\User;
+use App\Providers\RouteServiceProvider;
 use Illuminate\Auth\Access\AuthorizationException;
 use Illuminate\Auth\AuthenticationException;
 use Illuminate\Foundation\Exceptions\Handler as ExceptionHandler;
+use Illuminate\Session\TokenMismatchException;
 use Psr\Log\LogLevel;
 use RuntimeException;
 use Sentry\Laravel\Integration;
@@ -69,6 +71,11 @@ protected function unauthenticated($request, AuthenticationException $exception)
      */
     public function render($request, Throwable $e)
     {
+        // A duplicate login or 2FA submission carries a stale token on an already authenticated session, see https://github.com/coollabsio/coolify/issues/10670
+        if ($e instanceof TokenMismatchException && $request->routeIs('login.store', 'two-factor.login.store') && $request->user()) {
+            return redirect()->intended(RouteServiceProvider::HOME);
+        }
+
         // Handle authorization exceptions for API routes. Exceptions carrying
         // an explicit status (e.g. denyAsNotFound) keep it via parent::render.
         if ($e instanceof AuthorizationException && ! $e->hasStatus()) {
diff --git a/resources/views/auth/two-factor-challenge.blade.php b/resources/views/auth/two-factor-challenge.blade.php
index b15afc24d..10480b920 100644
--- a/resources/views/auth/two-factor-challenge.blade.php
+++ b/resources/views/auth/two-factor-challenge.blade.php
@@ -2,6 +2,14 @@
     <x-auth.shell title="Coolify" description="Verify your identity to finish signing in.">
         <div class="flex flex-col gap-4" x-data="{
             showRecovery: false,
+            submitting: false,
+            handleSubmit(event) {
+                if (this.submitting) {
+                    event.preventDefault();
+                }
+
+                this.submitting = true;
+            },
             submitAuthenticatorCode(event) {
                 event.target.value = event.target.value.replace(/\D/g, '').slice(0, 6);
 
@@ -30,7 +38,8 @@
                 <p x-show="showRecovery" x-cloak>Enter one of the recovery codes you saved when setting up two-factor authentication.</p>
             </div>
 
-            <form x-ref="challengeForm" action="/two-factor-challenge" method="POST" class="flex flex-col gap-4">
+            <form x-ref="challengeForm" action="/two-factor-challenge" method="POST" class="flex flex-col gap-4"
+                @submit="handleSubmit($event)">
                 @csrf
 
                 <div x-show="!showRecovery" class="flex flex-col gap-3">
@@ -54,7 +63,7 @@ class="mx-auto h-14 w-64 rounded-md border border-neutral-300 bg-white px-4 text
                     </button>
                 </div>
 
-                <x-forms.button class="w-full justify-center" type="submit" isHighlighted>
+                <x-forms.button class="w-full justify-center" type="submit" x-bind:disabled="submitting" isHighlighted>
                     Verify and continue
                 </x-forms.button>
             </form>
diff --git a/tests/Feature/Auth/TwoFactorChallengeAccessTest.php b/tests/Feature/Auth/TwoFactorChallengeAccessTest.php
index f0dd97cc3..a46f6b35c 100644
--- a/tests/Feature/Auth/TwoFactorChallengeAccessTest.php
+++ b/tests/Feature/Auth/TwoFactorChallengeAccessTest.php
@@ -3,7 +3,11 @@
 use App\Models\InstanceSettings;
 use App\Models\Team;
 use App\Models\User;
+use Illuminate\Contracts\Debug\ExceptionHandler;
 use Illuminate\Foundation\Testing\RefreshDatabase;
+use Illuminate\Http\Request;
+use Illuminate\Session\TokenMismatchException;
+use Illuminate\Support\Facades\Route;
 
 uses(RefreshDatabase::class);
 
@@ -78,3 +82,33 @@
     expect($view)->toContain('error-shell');
     expect($view)->not->toContain('url()->previous()');
 });
+
+it('redirects an authenticated stale two-factor submission home instead of showing 419', function () {
+    $request = Request::create('/two-factor-challenge', 'POST');
+    $request->setRouteResolver(fn () => Route::getRoutes()->match($request));
+    $request->setUserResolver(fn () => $this->user);
+
+    $response = app(ExceptionHandler::class)->render($request, new TokenMismatchException('CSRF token mismatch.'));
+
+    expect($response->getStatusCode())->toBe(302)
+        ->and($response->headers->get('Location'))->toBe(url('/'));
+});
+
+it('still returns 419 for a stale two-factor submission without an authenticated session', function () {
+    $request = Request::create('/two-factor-challenge', 'POST');
+    $request->setRouteResolver(fn () => Route::getRoutes()->match($request));
+
+    $response = app(ExceptionHandler::class)->render($request, new TokenMismatchException('CSRF token mismatch.'));
+
+    expect($response->getStatusCode())->toBe(419);
+});
+
+it('keeps the 419 for stale tokens on routes other than login and the two-factor challenge', function () {
+    $request = Request::create('/two-factor-challenge', 'GET');
+    $request->setRouteResolver(fn () => Route::getRoutes()->match($request));
+    $request->setUserResolver(fn () => $this->user);
+
+    $response = app(ExceptionHandler::class)->render($request, new TokenMismatchException('CSRF token mismatch.'));
+
+    expect($response->getStatusCode())->toBe(419);
+});
diff --git a/tests/v4/Browser/LoginTest.php b/tests/v4/Browser/LoginTest.php
index 7a6d6f2b7..df960a71b 100644
--- a/tests/v4/Browser/LoginTest.php
+++ b/tests/v4/Browser/LoginTest.php
@@ -4,6 +4,7 @@
 use App\Models\User;
 use Illuminate\Foundation\Testing\RefreshDatabase;
 use Illuminate\Support\Facades\Hash;
+use Laravel\Fortify\Fortify;
 
 uses(RefreshDatabase::class);
 
@@ -69,6 +70,43 @@
         ->screenshot(filename: 'login-invalid-credentials');
 });
 
+it('submits the automatic two factor challenge only once', function () {
+    config(['app.maintenance.driver' => 'file']);
+
+    $user = createRootUser();
+    $user->forceFill([
+        'two_factor_secret' => Fortify::currentEncrypter()->encrypt('JBSWY3DPEHPK3PXP'),
+        'two_factor_confirmed_at' => now(),
+    ])->save();
+
+    $page = visit('/login')
+        ->fill('email', 'test@example.com')
+        ->fill('password', 'password')
+        ->click('Login')
+        ->assertPathIs('/two-factor-challenge');
+
+    $page->script(<<<'JS'
+        window.acceptedTwoFactorSubmissions = 0;
+
+        document.querySelector('form[action="/two-factor-challenge"]').addEventListener('submit', (event) => {
+            if (!event.defaultPrevented) {
+                window.acceptedTwoFactorSubmissions++;
+            }
+
+            event.preventDefault();
+        });
+    JS);
+
+    $page->fill('code', '123456')
+        ->keys('code', 'Enter')
+        ->assertScript('window.acceptedTwoFactorSubmissions', 1)
+        ->assertDisabled('Verify and continue')
+        ->fill('code', '654321')
+        ->assertScript('window.acceptedTwoFactorSubmissions', 1)
+        ->assertNoJavaScriptErrors()
+        ->screenshot(filename: 'login-two-factor-enter-single-submission');
+});
+
 /**
  * Create the root user (id 0) with known credentials for browser login tests.
  */