diff --git a/core/modules/jsonapi/src/Controller/FileUpload.php b/core/modules/jsonapi/src/Controller/FileUpload.php
index 24676257c6..359768c968 100644
--- a/core/modules/jsonapi/src/Controller/FileUpload.php
+++ b/core/modules/jsonapi/src/Controller/FileUpload.php
@@ -5,6 +5,7 @@
 use Drupal\Core\Access\AccessResultReasonInterface;
 use Drupal\Core\Cache\CacheableMetadata;
 use Drupal\Core\Entity\EntityFieldManagerInterface;
+use Drupal\Core\Entity\Exception\UnknownFieldException;
 use Drupal\Core\Entity\FieldableEntityInterface;
 use Drupal\Core\Field\FieldDefinitionInterface;
 use Drupal\Core\File\Exception\FileException;
@@ -32,6 +33,7 @@
 use Symfony\Component\HttpFoundation\Response;
 use Symfony\Component\HttpKernel\Exception\AccessDeniedHttpException;
 use Symfony\Component\HttpKernel\Exception\HttpException;
+use Symfony\Component\HttpKernel\Exception\NotFoundHttpException;
 use Symfony\Component\HttpKernel\Exception\UnprocessableEntityHttpException;
 use Symfony\Component\HttpKernel\HttpKernelInterface;
 
@@ -239,7 +241,13 @@ public function handleFileUploadForNewResource(Request $request, ResourceType $r
    */
   protected function doHandleFileUpload(Request $request, ResourceType $resource_type, string $file_field_name): FileInterface {
     $file_field_name = $resource_type->getInternalName($file_field_name);
-    $field_definition = $this->fieldResolver->resolveFieldDefinition($resource_type->getEntityTypeId(), $resource_type->getBundle(), $file_field_name);
+
+    try {
+      $field_definition = $this->fieldResolver->resolveFieldDefinition($resource_type->getEntityTypeId(), $resource_type->getBundle(), $file_field_name);
+    }
+    catch (UnknownFieldException $e) {
+      throw new NotFoundHttpException($e->getMessage(), $e);
+    }
 
     $this->ensureFileUploadAccess($field_definition);
 
diff --git a/core/modules/jsonapi/tests/src/Functional/ResourceTestBase.php b/core/modules/jsonapi/tests/src/Functional/ResourceTestBase.php
index d7dae50d0c..01aae8e0dc 100644
--- a/core/modules/jsonapi/tests/src/Functional/ResourceTestBase.php
+++ b/core/modules/jsonapi/tests/src/Functional/ResourceTestBase.php
@@ -65,6 +65,7 @@ abstract class ResourceTestBase extends BrowserTestBase {
     'rest_test',
     'jsonapi_test_field_access',
     'text',
+    'file',
   ];
 
   /**
diff --git a/core/modules/jsonapi/tests/src/Kernel/Context/FieldResolverTest.php b/core/modules/jsonapi/tests/src/Kernel/Context/FieldResolverTest.php
index fc274647fa..9cddbe0db0 100644
--- a/core/modules/jsonapi/tests/src/Kernel/Context/FieldResolverTest.php
+++ b/core/modules/jsonapi/tests/src/Kernel/Context/FieldResolverTest.php
@@ -24,6 +24,7 @@ class FieldResolverTest extends JsonapiKernelTestBase {
     'field',
     'text',
     'user',
+    'file',
   ];
 
   /**
diff --git a/core/modules/jsonapi/tests/src/Kernel/Controller/EntityResourceTest.php b/core/modules/jsonapi/tests/src/Kernel/Controller/EntityResourceTest.php
index 859cb80599..ec56dd9f29 100644
--- a/core/modules/jsonapi/tests/src/Kernel/Controller/EntityResourceTest.php
+++ b/core/modules/jsonapi/tests/src/Kernel/Controller/EntityResourceTest.php
@@ -46,6 +46,7 @@ class EntityResourceTest extends JsonapiKernelTestBase {
     'serialization',
     'system',
     'user',
+    'file',
   ];
 
   /**
diff --git a/core/modules/jsonapi/tests/src/Kernel/EventSubscriber/ResourceObjectNormalizerCacherTest.php b/core/modules/jsonapi/tests/src/Kernel/EventSubscriber/ResourceObjectNormalizerCacherTest.php
index e715edc47e..67937d79b1 100644
--- a/core/modules/jsonapi/tests/src/Kernel/EventSubscriber/ResourceObjectNormalizerCacherTest.php
+++ b/core/modules/jsonapi/tests/src/Kernel/EventSubscriber/ResourceObjectNormalizerCacherTest.php
@@ -27,6 +27,7 @@ class ResourceObjectNormalizerCacherTest extends KernelTestBase {
     'serialization',
     'jsonapi',
     'user',
+    'file',
   ];
 
   /**
diff --git a/core/modules/jsonapi/tests/src/Kernel/Normalizer/FieldItemNormalizerTest.php b/core/modules/jsonapi/tests/src/Kernel/Normalizer/FieldItemNormalizerTest.php
index cb40e712b5..f290f971db 100644
--- a/core/modules/jsonapi/tests/src/Kernel/Normalizer/FieldItemNormalizerTest.php
+++ b/core/modules/jsonapi/tests/src/Kernel/Normalizer/FieldItemNormalizerTest.php
@@ -26,6 +26,7 @@ class FieldItemNormalizerTest extends JsonapiKernelTestBase {
     'link',
     'entity_test',
     'serialization',
+    'file',
   ];
 
   /**
diff --git a/core/modules/jsonapi/tests/src/Kernel/Normalizer/LinkCollectionNormalizerTest.php b/core/modules/jsonapi/tests/src/Kernel/Normalizer/LinkCollectionNormalizerTest.php
index 4282b62947..8dc4cb8ebb 100644
--- a/core/modules/jsonapi/tests/src/Kernel/Normalizer/LinkCollectionNormalizerTest.php
+++ b/core/modules/jsonapi/tests/src/Kernel/Normalizer/LinkCollectionNormalizerTest.php
@@ -53,6 +53,7 @@ class LinkCollectionNormalizerTest extends KernelTestBase {
     'serialization',
     'system',
     'user',
+    'file',
   ];
 
   /**
diff --git a/core/modules/jsonapi/tests/src/Kernel/ResourceType/RelatedResourceTypesTest.php b/core/modules/jsonapi/tests/src/Kernel/ResourceType/RelatedResourceTypesTest.php
index 3ee33a9c6e..f6d56d70a9 100644
--- a/core/modules/jsonapi/tests/src/Kernel/ResourceType/RelatedResourceTypesTest.php
+++ b/core/modules/jsonapi/tests/src/Kernel/ResourceType/RelatedResourceTypesTest.php
@@ -25,6 +25,7 @@ class RelatedResourceTypesTest extends JsonapiKernelTestBase {
     'system',
     'user',
     'field',
+    'file',
   ];
 
   /**
diff --git a/core/modules/jsonapi/tests/src/Kernel/ResourceType/ResourceTypeRepositoryTest.php b/core/modules/jsonapi/tests/src/Kernel/ResourceType/ResourceTypeRepositoryTest.php
index 5503967191..41acfe54b9 100644
--- a/core/modules/jsonapi/tests/src/Kernel/ResourceType/ResourceTypeRepositoryTest.php
+++ b/core/modules/jsonapi/tests/src/Kernel/ResourceType/ResourceTypeRepositoryTest.php
@@ -25,6 +25,7 @@ class ResourceTypeRepositoryTest extends JsonapiKernelTestBase {
     'system',
     'user',
     'jsonapi_test_resource_type_building',
+    'file',
   ];
 
   /**
diff --git a/core/modules/jsonapi/tests/src/Kernel/Revisions/VersionNegotiatorTest.php b/core/modules/jsonapi/tests/src/Kernel/Revisions/VersionNegotiatorTest.php
index ce8fabf3df..eb87fc1dfe 100644
--- a/core/modules/jsonapi/tests/src/Kernel/Revisions/VersionNegotiatorTest.php
+++ b/core/modules/jsonapi/tests/src/Kernel/Revisions/VersionNegotiatorTest.php
@@ -64,6 +64,7 @@ class VersionNegotiatorTest extends JsonapiKernelTestBase {
     'serialization',
     'system',
     'user',
+    'file',
   ];
 
   /**
diff --git a/core/modules/jsonapi/tests/src/Kernel/Serializer/SerializerTest.php b/core/modules/jsonapi/tests/src/Kernel/Serializer/SerializerTest.php
index b55b25b98f..54cbc83fd9 100644
--- a/core/modules/jsonapi/tests/src/Kernel/Serializer/SerializerTest.php
+++ b/core/modules/jsonapi/tests/src/Kernel/Serializer/SerializerTest.php
@@ -33,6 +33,7 @@ class SerializerTest extends JsonapiKernelTestBase {
     'text',
     'filter',
     'jsonapi_test_data_type',
+    'file',
   ];
 
   /**