diff --git a/system/Commands/Utilities/Routes.php b/system/Commands/Utilities/Routes.php
index 210d1e11c5f7..26ad9b2a689e 100644
--- a/system/Commands/Utilities/Routes.php
+++ b/system/Commands/Utilities/Routes.php
@@ -13,12 +13,13 @@
 
 use CodeIgniter\CLI\BaseCommand;
 use CodeIgniter\CLI\CLI;
+use CodeIgniter\Commands\Utilities\Routes\AutoRouteCollector;
 use Config\Services;
 
 /**
- * Lists all of the user-defined routes. This will include any Routes files
- * that can be discovered, but will NOT include any routes that are not defined
- * in a routes file, but are instead discovered through auto-routing.
+ * Lists all the routes. This will include any Routes files
+ * that can be discovered, and will include routes that are not defined
+ * in routes files, but are instead discovered through auto-routing.
  */
 class Routes extends BaseCommand
 {
@@ -101,6 +102,15 @@ public function run(array $params)
             }
         }
 
+        if ($collection->shouldAutoRoute()) {
+            $autoRouteCollector = new AutoRouteCollector(
+                $collection->getDefaultNamespace(),
+                $collection->getDefaultController(),
+                $collection->getDefaultMethod()
+            );
+            $tbody = [...$tbody, ...$autoRouteCollector->get()];
+        }
+
         $thead = [
             'Method',
             'Route',
diff --git a/system/Commands/Utilities/Routes/AutoRouteCollector.php b/system/Commands/Utilities/Routes/AutoRouteCollector.php
new file mode 100644
index 000000000000..a3254adb6a57
--- /dev/null
+++ b/system/Commands/Utilities/Routes/AutoRouteCollector.php
@@ -0,0 +1,65 @@
+<?php
+
+/**
+ * This file is part of CodeIgniter 4 framework.
+ *
+ * (c) CodeIgniter Foundation <admin@codeigniter.com>
+ *
+ * For the full copyright and license information, please view
+ * the LICENSE file that was distributed with this source code.
+ */
+
+namespace CodeIgniter\Commands\Utilities\Routes;
+
+/**
+ * Collects data for auto route listing.
+ */
+final class AutoRouteCollector
+{
+    /**
+     * @var string namespace to search
+     */
+    private string $namespace;
+
+    private string $defaultController;
+    private string $defaultMethod;
+
+    /**
+     * @param string $namespace namespace to search
+     */
+    public function __construct(string $namespace, string $defaultController, string $defaultMethod)
+    {
+        $this->namespace         = $namespace;
+        $this->defaultController = $defaultController;
+        $this->defaultMethod     = $defaultMethod;
+    }
+
+    /**
+     * @return list<list<string>>
+     */
+    public function get(): array
+    {
+        $finder = new ControllerFinder($this->namespace);
+        $reader = new ControllerMethodReader($this->namespace);
+
+        $tbody = [];
+
+        foreach ($finder->find() as $class) {
+            $output = $reader->read(
+                $class,
+                $this->defaultController,
+                $this->defaultMethod
+            );
+
+            foreach ($output as $item) {
+                $tbody[] = [
+                    'auto',
+                    $item['route'],
+                    $item['handler'],
+                ];
+            }
+        }
+
+        return $tbody;
+    }
+}
diff --git a/system/Commands/Utilities/Routes/ControllerFinder.php b/system/Commands/Utilities/Routes/ControllerFinder.php
new file mode 100644
index 000000000000..9e6dd5ca2005
--- /dev/null
+++ b/system/Commands/Utilities/Routes/ControllerFinder.php
@@ -0,0 +1,75 @@
+<?php
+
+/**
+ * This file is part of CodeIgniter 4 framework.
+ *
+ * (c) CodeIgniter Foundation <admin@codeigniter.com>
+ *
+ * For the full copyright and license information, please view
+ * the LICENSE file that was distributed with this source code.
+ */
+
+namespace CodeIgniter\Commands\Utilities\Routes;
+
+use CodeIgniter\Autoloader\FileLocator;
+use CodeIgniter\Config\Services;
+
+/**
+ * Finds all controllers in a namespace for auto route listing.
+ */
+final class ControllerFinder
+{
+    /**
+     * @var string namespace to search
+     */
+    private string $namespace;
+
+    private FileLocator $locator;
+
+    /**
+     * @param string $namespace namespace to search
+     */
+    public function __construct(string $namespace)
+    {
+        $this->namespace = $namespace;
+        $this->locator   = Services::locator();
+    }
+
+    /**
+     * @return class-string[]
+     */
+    public function find(): array
+    {
+        $nsArray = explode('\\', trim($this->namespace, '\\'));
+        $count   = count($nsArray);
+        $ns      = '';
+
+        for ($i = 0; $i < $count; $i++) {
+            $ns .= '\\' . array_shift($nsArray);
+            $path = implode('\\', $nsArray);
+
+            $files = $this->locator->listNamespaceFiles($ns, $path);
+
+            if ($files !== []) {
+                break;
+            }
+        }
+
+        $classes = [];
+
+        foreach ($files as $file) {
+            if (\is_file($file)) {
+                $classnameOrEmpty = $this->locator->getClassname($file);
+
+                if ($classnameOrEmpty !== '') {
+                    /** @var class-string $classname */
+                    $classname = $classnameOrEmpty;
+
+                    $classes[] = $classname;
+                }
+            }
+        }
+
+        return $classes;
+    }
+}
diff --git a/system/Commands/Utilities/Routes/ControllerMethodReader.php b/system/Commands/Utilities/Routes/ControllerMethodReader.php
new file mode 100644
index 000000000000..0e9549f2b88a
--- /dev/null
+++ b/system/Commands/Utilities/Routes/ControllerMethodReader.php
@@ -0,0 +1,175 @@
+<?php
+
+/**
+ * This file is part of CodeIgniter 4 framework.
+ *
+ * (c) CodeIgniter Foundation <admin@codeigniter.com>
+ *
+ * For the full copyright and license information, please view
+ * the LICENSE file that was distributed with this source code.
+ */
+
+namespace CodeIgniter\Commands\Utilities\Routes;
+
+use ReflectionClass;
+use ReflectionMethod;
+
+/**
+ * Reads a controller and returns a list of auto route listing.
+ */
+final class ControllerMethodReader
+{
+    /**
+     * @var string the default namespace
+     */
+    private string $namespace;
+
+    /**
+     * @param string $namespace the default namespace
+     */
+    public function __construct(string $namespace)
+    {
+        $this->namespace = $namespace;
+    }
+
+    /**
+     * @param class-string $class
+     *
+     * @return list<array{route: string, handler: string}>
+     */
+    public function read(string $class, string $defaultController = 'Home', string $defaultMethod = 'index'): array
+    {
+        $reflection = new ReflectionClass($class);
+
+        if ($reflection->isAbstract()) {
+            return [];
+        }
+
+        $classname      = $reflection->getName();
+        $classShortname = $reflection->getShortName();
+
+        $output     = [];
+        $uriByClass = $this->getUriByClass($classname);
+
+        if ($this->hasRemap($reflection)) {
+            $methodName = '_remap';
+
+            $routeWithoutController = $this->getRouteWithoutController(
+                $classShortname,
+                $defaultController,
+                $uriByClass,
+                $classname,
+                $methodName
+            );
+            $output = [...$output, ...$routeWithoutController];
+
+            $output[] = [
+                'route'   => $uriByClass . '[/...]',
+                'handler' => '\\' . $classname . '::' . $methodName,
+            ];
+
+            return $output;
+        }
+
+        foreach ($reflection->getMethods(ReflectionMethod::IS_PUBLIC) as $method) {
+            $methodName = $method->getName();
+
+            $route = $uriByClass . '/' . $methodName;
+
+            // Exclude BaseController and initController
+            // See system/Config/Routes.php
+            if (preg_match('#\AbaseController.*#', $route) === 1) {
+                continue;
+            }
+            if (preg_match('#.*/initController\z#', $route) === 1) {
+                continue;
+            }
+
+            if ($methodName === $defaultMethod) {
+                $routeWithoutController = $this->getRouteWithoutController(
+                    $classShortname,
+                    $defaultController,
+                    $uriByClass,
+                    $classname,
+                    $methodName
+                );
+                $output = [...$output, ...$routeWithoutController];
+
+                $output[] = [
+                    'route'   => $uriByClass,
+                    'handler' => '\\' . $classname . '::' . $methodName,
+                ];
+            }
+
+            $output[] = [
+                'route'   => $route . '[/...]',
+                'handler' => '\\' . $classname . '::' . $methodName,
+            ];
+        }
+
+        return $output;
+    }
+
+    /**
+     * Whether the class has a _remap() method.
+     */
+    private function hasRemap(ReflectionClass $class): bool
+    {
+        if ($class->hasMethod('_remap')) {
+            $remap = $class->getMethod('_remap');
+
+            return $remap->isPublic();
+        }
+
+        return false;
+    }
+
+    /**
+     * @param class-string $classname
+     *
+     * @return string URI path part from the folder(s) and controller
+     */
+    private function getUriByClass(string $classname): string
+    {
+        // remove the namespace
+        $pattern = '/' . preg_quote($this->namespace, '/') . '/';
+        $class   = ltrim(preg_replace($pattern, '', $classname), '\\');
+
+        $classParts = explode('\\', $class);
+        $classPath  = '';
+
+        foreach ($classParts as $part) {
+            // make the first letter lowercase, because auto routing makes
+            // the URI path's first letter uppercase and search the controller
+            $classPath .= lcfirst($part) . '/';
+        }
+
+        return rtrim($classPath, '/');
+    }
+
+    /**
+     * Gets a route without default controller.
+     */
+    private function getRouteWithoutController(
+        string $classShortname,
+        string $defaultController,
+        string $uriByClass,
+        string $classname,
+        string $methodName
+    ): array {
+        $output = [];
+
+        if ($classShortname === $defaultController) {
+            $pattern                = '#' . preg_quote(lcfirst($defaultController), '#') . '\z#';
+            $routeWithoutController = rtrim(preg_replace($pattern, '', $uriByClass), '/');
+            $routeWithoutController = $routeWithoutController ?: '/';
+
+            $output[] = [
+                'route'   => $routeWithoutController,
+                'handler' => '\\' . $classname . '::' . $methodName,
+            ];
+        }
+
+        return $output;
+    }
+}
diff --git a/tests/_support/Controllers/Hello.php b/tests/_support/Controllers/Hello.php
index cc63814d7e09..ac9f421b55d1 100644
--- a/tests/_support/Controllers/Hello.php
+++ b/tests/_support/Controllers/Hello.php
@@ -9,7 +9,7 @@
  * the LICENSE file that was distributed with this source code.
  */
 
-namespace App\Controllers;
+namespace Tests\Support\Controllers;
 
 use CodeIgniter\Controller;
 
diff --git a/tests/_support/Controllers/Remap.php b/tests/_support/Controllers/Remap.php
new file mode 100644
index 000000000000..1489a80aa776
--- /dev/null
+++ b/tests/_support/Controllers/Remap.php
@@ -0,0 +1,36 @@
+<?php
+
+/**
+ * This file is part of CodeIgniter 4 framework.
+ *
+ * (c) CodeIgniter Foundation <admin@codeigniter.com>
+ *
+ * For the full copyright and license information, please view
+ * the LICENSE file that was distributed with this source code.
+ */
+
+namespace Tests\Support\Controllers;
+
+use CodeIgniter\Controller;
+
+class Remap extends Controller
+{
+    public function _remap($method, ...$params)
+    {
+        if ($method === 'xyz') {
+            return $this->abc();
+        }
+
+        return $this->index();
+    }
+
+    public function index()
+    {
+        return 'index';
+    }
+
+    public function abc()
+    {
+        return 'abc';
+    }
+}
diff --git a/tests/system/Commands/Utilities/Routes/AutoRouteCollectorTest.php b/tests/system/Commands/Utilities/Routes/AutoRouteCollectorTest.php
new file mode 100644
index 000000000000..dd1c5db46b5f
--- /dev/null
+++ b/tests/system/Commands/Utilities/Routes/AutoRouteCollectorTest.php
@@ -0,0 +1,121 @@
+<?php
+
+/**
+ * This file is part of CodeIgniter 4 framework.
+ *
+ * (c) CodeIgniter Foundation <admin@codeigniter.com>
+ *
+ * For the full copyright and license information, please view
+ * the LICENSE file that was distributed with this source code.
+ */
+
+namespace CodeIgniter\Commands\Utilities\Routes;
+
+use CodeIgniter\Test\CIUnitTestCase;
+
+/**
+ * @internal
+ */
+final class AutoRouteCollectorTest extends CIUnitTestCase
+{
+    public function testGet()
+    {
+        $namespace = 'Tests\Support\Controllers';
+        $collector = new AutoRouteCollector(
+            $namespace,
+            'Home',
+            'index',
+        );
+
+        $routes = $collector->get();
+
+        $expected = [
+            0 => [
+                0 => 'auto',
+                1 => 'hello',
+                2 => '\\Tests\\Support\\Controllers\\Hello::index',
+            ],
+            1 => [
+                0 => 'auto',
+                1 => 'hello/index[/...]',
+                2 => '\\Tests\\Support\\Controllers\\Hello::index',
+            ],
+            2 => [
+                0 => 'auto',
+                1 => 'popcorn',
+                2 => '\\Tests\\Support\\Controllers\\Popcorn::index',
+            ],
+            3 => [
+                0 => 'auto',
+                1 => 'popcorn/index[/...]',
+                2 => '\\Tests\\Support\\Controllers\\Popcorn::index',
+            ],
+            4 => [
+                0 => 'auto',
+                1 => 'popcorn/pop[/...]',
+                2 => '\\Tests\\Support\\Controllers\\Popcorn::pop',
+            ],
+            5 => [
+                0 => 'auto',
+                1 => 'popcorn/popper[/...]',
+                2 => '\\Tests\\Support\\Controllers\\Popcorn::popper',
+            ],
+            6 => [
+                0 => 'auto',
+                1 => 'popcorn/weasel[/...]',
+                2 => '\\Tests\\Support\\Controllers\\Popcorn::weasel',
+            ],
+            7 => [
+                0 => 'auto',
+                1 => 'popcorn/oops[/...]',
+                2 => '\\Tests\\Support\\Controllers\\Popcorn::oops',
+            ],
+            8 => [
+                0 => 'auto',
+                1 => 'popcorn/goaway[/...]',
+                2 => '\\Tests\\Support\\Controllers\\Popcorn::goaway',
+            ],
+            9 => [
+                0 => 'auto',
+                1 => 'popcorn/index3[/...]',
+                2 => '\\Tests\\Support\\Controllers\\Popcorn::index3',
+            ],
+            10 => [
+                0 => 'auto',
+                1 => 'popcorn/canyon[/...]',
+                2 => '\\Tests\\Support\\Controllers\\Popcorn::canyon',
+            ],
+            11 => [
+                0 => 'auto',
+                1 => 'popcorn/cat[/...]',
+                2 => '\\Tests\\Support\\Controllers\\Popcorn::cat',
+            ],
+            12 => [
+                0 => 'auto',
+                1 => 'popcorn/json[/...]',
+                2 => '\\Tests\\Support\\Controllers\\Popcorn::json',
+            ],
+            13 => [
+                0 => 'auto',
+                1 => 'popcorn/xml[/...]',
+                2 => '\\Tests\\Support\\Controllers\\Popcorn::xml',
+            ],
+            14 => [
+                0 => 'auto',
+                1 => 'popcorn/toindex[/...]',
+                2 => '\\Tests\\Support\\Controllers\\Popcorn::toindex',
+            ],
+            15 => [
+                0 => 'auto',
+                1 => 'popcorn/echoJson[/...]',
+                2 => '\\Tests\\Support\\Controllers\\Popcorn::echoJson',
+            ],
+            16 => [
+                0 => 'auto',
+                1 => 'remap[/...]',
+                2 => '\\Tests\\Support\\Controllers\\Remap::_remap',
+            ],
+        ];
+        $this->assertSame($expected, $routes);
+    }
+}
diff --git a/tests/system/Commands/Utilities/Routes/ControllerFinderTest.php b/tests/system/Commands/Utilities/Routes/ControllerFinderTest.php
new file mode 100644
index 000000000000..676a1869b1b3
--- /dev/null
+++ b/tests/system/Commands/Utilities/Routes/ControllerFinderTest.php
@@ -0,0 +1,31 @@
+<?php
+
+/**
+ * This file is part of CodeIgniter 4 framework.
+ *
+ * (c) CodeIgniter Foundation <admin@codeigniter.com>
+ *
+ * For the full copyright and license information, please view
+ * the LICENSE file that was distributed with this source code.
+ */
+
+namespace CodeIgniter\Commands\Utilities\Routes;
+
+use CodeIgniter\Test\CIUnitTestCase;
+
+/**
+ * @internal
+ */
+final class ControllerFinderTest extends CIUnitTestCase
+{
+    public function testFind()
+    {
+        $namespace = 'Tests\Support\Controllers';
+        $finder    = new ControllerFinder($namespace);
+
+        $controllers = $finder->find();
+
+        $this->assertCount(3, $controllers);
+        $this->assertSame('Tests\Support\Controllers\Hello', $controllers[0]);
+    }
+}
diff --git a/tests/system/Commands/Utilities/Routes/ControllerMethodReaderTest.php b/tests/system/Commands/Utilities/Routes/ControllerMethodReaderTest.php
new file mode 100644
index 000000000000..a899b9c44b73
--- /dev/null
+++ b/tests/system/Commands/Utilities/Routes/ControllerMethodReaderTest.php
@@ -0,0 +1,106 @@
+<?php
+
+/**
+ * This file is part of CodeIgniter 4 framework.
+ *
+ * (c) CodeIgniter Foundation <admin@codeigniter.com>
+ *
+ * For the full copyright and license information, please view
+ * the LICENSE file that was distributed with this source code.
+ */
+
+namespace CodeIgniter\Commands\Utilities\Routes;
+
+use CodeIgniter\Test\CIUnitTestCase;
+use Tests\Support\Controllers\Popcorn;
+use Tests\Support\Controllers\Remap;
+
+/**
+ * @internal
+ */
+final class ControllerMethodReaderTest extends CIUnitTestCase
+{
+    public function testRead()
+    {
+        $namespace = 'Tests\Support\Controllers';
+        $reader    = new ControllerMethodReader($namespace);
+
+        $routes = $reader->read(Popcorn::class);
+
+        $expected = [
+            0 => [
+                'route'   => 'popcorn',
+                'handler' => '\\Tests\\Support\\Controllers\\Popcorn::index',
+            ],
+            1 => [
+                'route'   => 'popcorn/index[/...]',
+                'handler' => '\\Tests\\Support\\Controllers\\Popcorn::index',
+            ],
+            2 => [
+                'route'   => 'popcorn/pop[/...]',
+                'handler' => '\\Tests\\Support\\Controllers\\Popcorn::pop',
+            ],
+            3 => [
+                'route'   => 'popcorn/popper[/...]',
+                'handler' => '\\Tests\\Support\\Controllers\\Popcorn::popper',
+            ],
+            4 => [
+                'route'   => 'popcorn/weasel[/...]',
+                'handler' => '\\Tests\\Support\\Controllers\\Popcorn::weasel',
+            ],
+            5 => [
+                'route'   => 'popcorn/oops[/...]',
+                'handler' => '\\Tests\\Support\\Controllers\\Popcorn::oops',
+            ],
+            6 => [
+                'route'   => 'popcorn/goaway[/...]',
+                'handler' => '\\Tests\\Support\\Controllers\\Popcorn::goaway',
+            ],
+            7 => [
+                'route'   => 'popcorn/index3[/...]',
+                'handler' => '\\Tests\\Support\\Controllers\\Popcorn::index3',
+            ],
+            8 => [
+                'route'   => 'popcorn/canyon[/...]',
+                'handler' => '\\Tests\\Support\\Controllers\\Popcorn::canyon',
+            ],
+            9 => [
+                'route'   => 'popcorn/cat[/...]',
+                'handler' => '\\Tests\\Support\\Controllers\\Popcorn::cat',
+            ],
+            10 => [
+                'route'   => 'popcorn/json[/...]',
+                'handler' => '\\Tests\\Support\\Controllers\\Popcorn::json',
+            ],
+            11 => [
+                'route'   => 'popcorn/xml[/...]',
+                'handler' => '\\Tests\\Support\\Controllers\\Popcorn::xml',
+            ],
+            12 => [
+                'route'   => 'popcorn/toindex[/...]',
+                'handler' => '\\Tests\\Support\\Controllers\\Popcorn::toindex',
+            ],
+            13 => [
+                'route'   => 'popcorn/echoJson[/...]',
+                'handler' => '\\Tests\\Support\\Controllers\\Popcorn::echoJson',
+            ],
+        ];
+        $this->assertSame($expected, $routes);
+    }
+
+    public function testReadControllerWithRemap()
+    {
+        $namespace = 'Tests\Support\Controllers';
+        $reader    = new ControllerMethodReader($namespace);
+
+        $routes = $reader->read(Remap::class);
+
+        $expected = [
+            0 => [
+                'route'   => 'remap[/...]',
+                'handler' => '\\Tests\\Support\\Controllers\\Remap::_remap',
+            ],
+        ];
+        $this->assertSame($expected, $routes);
+    }
+}