diff --git a/VERSION.txt b/VERSION.txt
index 994f0ca6e73..4816ad91d9b 100644
--- a/VERSION.txt
+++ b/VERSION.txt
@@ -16,4 +16,4 @@
 // @license       https://opensource.org/licenses/mit-license.php MIT License
 // +--------------------------------------------------------------------------------------------+ //
 ////////////////////////////////////////////////////////////////////////////////////////////////////
-4.5.9
+4.5.10
diff --git a/src/Routing/RouteCollection.php b/src/Routing/RouteCollection.php
index 2f3988cf601..c91e5ba9e6c 100644
--- a/src/Routing/RouteCollection.php
+++ b/src/Routing/RouteCollection.php
@@ -225,7 +225,7 @@ public function parseRequest(ServerRequestInterface $request): array
                 }
                 if ($uri->getQuery()) {
                     parse_str($uri->getQuery(), $queryParameters);
-                    $r['?'] = $queryParameters;
+                    $r['?'] = array_merge($r['?'] ?? [], $queryParameters);
                 }
 
                 return $r;
diff --git a/tests/TestCase/Routing/RouteCollectionTest.php b/tests/TestCase/Routing/RouteCollectionTest.php
index 692b209c7f8..096f960e2c8 100644
--- a/tests/TestCase/Routing/RouteCollectionTest.php
+++ b/tests/TestCase/Routing/RouteCollectionTest.php
@@ -24,6 +24,7 @@
 use Cake\Routing\RouteCollection;
 use Cake\TestSuite\TestCase;
 use RuntimeException;
+use TestApp\Routing\Route\AddQueryParamRoute;
 
 class RouteCollectionTest extends TestCase
 {
@@ -138,8 +139,8 @@ public function testParse(): void
             $this->assertEquals($expected, $result);
         });
     }
-
     /**
+
      * Test parse() handling query strings.
      */
     public function testParseQueryString(): void
@@ -352,6 +353,31 @@ public function testParseRequestQueryString(): void
         $this->assertEquals($expected, $result);
     }
 
+    /**
+     * Test parseRequest() handling query strings.
+     */
+    public function testParseRequestQueryStringFromRoute(): void
+    {
+        $routes = new RouteBuilder($this->collection, '/');
+        $routes->connect(
+            '/test',
+            ['controller' => 'Articles', 'action' => 'view'],
+            ['routeClass' => AddQueryParamRoute::class],
+        );
+        $request = new ServerRequest(['url' => '/test?y=2']);
+        $result = $this->collection->parseRequest($request);
+        unset($result['_route']);
+        $expected = [
+            'controller' => 'Articles',
+            'action' => 'view',
+            'pass' => [],
+            'plugin' => null,
+            '_matchedRoute' => '/test',
+            '?' => ['x' => '1', 'y' => '2'],
+        ];
+        $this->assertEquals($expected, $result);
+    }
+
     /**
      * Test parseRequest() checks host conditions
      */
diff --git a/tests/test_app/TestApp/Routing/Route/AddQueryParamRoute.php b/tests/test_app/TestApp/Routing/Route/AddQueryParamRoute.php
new file mode 100644
index 00000000000..06e8075e7c9
--- /dev/null
+++ b/tests/test_app/TestApp/Routing/Route/AddQueryParamRoute.php
@@ -0,0 +1,20 @@
+<?php
+declare(strict_types=1);
+
+namespace TestApp\Routing\Route;
+
+use Cake\Routing\Route\Route;
+use Psr\Http\Message\ServerRequestInterface;
+
+class AddQueryParamRoute extends Route
+{
+    public function parseRequest(ServerRequestInterface $request): ?array
+    {
+        $params = parent::parseRequest($request);
+        if (is_array($params)) {
+            $params['?']['x'] = '1';
+        }
+
+        return $params;
+    }
+}