diff --git a/CHANGELOG.md b/CHANGELOG.md
index ef9fddde27b..03fa16838b3 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -29,6 +29,7 @@
 * Deprecate `allow_plain_identifiers` option (#4167)
 * Exception: Add the ability to customize multiple status codes based on the validation exception (#4017)
 * GraphQL: Fix graphql fetching with Elasticsearch (#4217)
+* ApiLoader: Support `_format` resolving (#4292)
 
 ## 2.6.5
 
diff --git a/src/Bridge/Symfony/Routing/ApiLoader.php b/src/Bridge/Symfony/Routing/ApiLoader.php
index d7390fd7bd8..9e03264ce9d 100644
--- a/src/Bridge/Symfony/Routing/ApiLoader.php
+++ b/src/Bridge/Symfony/Routing/ApiLoader.php
@@ -128,7 +128,7 @@ public function load($data, $type = null): RouteCollection
                     $operation['path'],
                     [
                         '_controller' => $controller,
-                        '_format' => null,
+                        '_format' => $operation['defaults']['_format'] ?? null,
                         '_stateless' => $operation['stateless'] ?? $resourceMetadata->getAttribute('stateless'),
                         '_api_resource_class' => $operation['resource_class'],
                         '_api_identifiers' => $operation['identifiers'],
@@ -241,7 +241,7 @@ private function addRoute(RouteCollection $routeCollection, string $resourceClas
             $path,
             [
                 '_controller' => $controller,
-                '_format' => null,
+                '_format' => $operation['defaults']['_format'] ?? null,
                 '_stateless' => $operation['stateless'],
                 '_api_resource_class' => $resourceClass,
                 '_api_identifiers' => $operation['identifiers'],
diff --git a/tests/Bridge/Symfony/Routing/ApiLoaderTest.php b/tests/Bridge/Symfony/Routing/ApiLoaderTest.php
index aae3a3b66eb..686763b32e6 100644
--- a/tests/Bridge/Symfony/Routing/ApiLoaderTest.php
+++ b/tests/Bridge/Symfony/Routing/ApiLoaderTest.php
@@ -60,7 +60,7 @@ public function testApiLoader()
         ]);
         //custom operations
         $resourceMetadata = $resourceMetadata->withCollectionOperations([
-            'my_op' => ['method' => 'GET', 'controller' => 'some.service.name', 'requirements' => ['_format' => 'a valid format'], 'defaults' => ['my_default' => 'default_value'], 'condition' => "request.headers.get('User-Agent') matches '/firefox/i'", 'stateless' => null], //with controller
+            'my_op' => ['method' => 'GET', 'controller' => 'some.service.name', 'requirements' => ['_format' => 'a valid format'], 'defaults' => ['my_default' => 'default_value', '_format' => 'a valid format'], 'condition' => "request.headers.get('User-Agent') matches '/firefox/i'", 'stateless' => null], //with controller
             'my_second_op' => ['method' => 'POST', 'options' => ['option' => 'option_value'], 'host' => '{subdomain}.api-platform.com', 'schemes' => ['https'], 'stateless' => null], //without controller, takes the default one
             'my_path_op' => ['method' => 'GET', 'path' => 'some/custom/path', 'stateless' => null], //custom path
             'my_stateless_op' => ['method' => 'GET', 'stateless' => true],
@@ -87,7 +87,7 @@ public function testApiLoader()
         );
 
         $this->assertEquals(
-            $this->getRoute('/dummies.{_format}', 'some.service.name', DummyEntity::class, 'my_op', ['GET'], true, ['_format' => 'a valid format'], ['my_default' => 'default_value', '_stateless' => null], [], '', [], "request.headers.get('User-Agent') matches '/firefox/i'"),
+            $this->getRoute('/dummies.{_format}', 'some.service.name', DummyEntity::class, 'my_op', ['GET'], true, ['_format' => 'a valid format'], ['my_default' => 'default_value', '_format' => 'a valid format', '_stateless' => null], [], '', [], "request.headers.get('User-Agent') matches '/firefox/i'"),
             $routeCollection->get('api_dummies_my_op_collection')
         );
 
@@ -318,7 +318,7 @@ private function getRoute(string $path, string $controller, string $resourceClas
             $path,
             [
                 '_controller' => $controller,
-                '_format' => null,
+                '_format' => $extraDefaults['_format'] ?? null,
                 '_api_resource_class' => $resourceClass,
                 '_api_identifiers' => ['id'],
                 '_api_has_composite_identifier' => false,
@@ -339,7 +339,7 @@ private function getSubresourceRoute(string $path, string $controller, string $r
             $path,
             [
                 '_controller' => $controller,
-                '_format' => null,
+                '_format' => $extraDefaults['_format'] ?? null,
                 '_api_resource_class' => $resourceClass,
                 '_api_subresource_operation_name' => $operationName,
                 '_api_subresource_context' => $context,