diff --git a/wagtail/documents/models.py b/wagtail/documents/models.py
index 445eb6c848..e84936f371 100644
--- a/wagtail/documents/models.py
+++ b/wagtail/documents/models.py
@@ -4,6 +4,7 @@ from contextlib import contextmanager
 from mimetypes import guess_type
 
 from django.conf import settings
+from django.core.exceptions import ValidationError
 from django.core.validators import FileExtensionValidator
 from django.db import models
 from django.dispatch import Signal
@@ -71,7 +72,10 @@ class AbstractDocument(CollectionMember, index.Indexed, models.Model):
         allowed_extensions = getattr(settings, "WAGTAILDOCS_EXTENSIONS", None)
         if allowed_extensions:
             validate = FileExtensionValidator(allowed_extensions)
-            validate(self.file)
+            try:
+                validate(self.file)
+            except ValidationError as e:
+                raise ValidationError({"file": e.messages[0]})
 
     def is_stored_locally(self):
         """
diff --git a/wagtail/documents/tests/test_models.py b/wagtail/documents/tests/test_models.py
index e7a88ab8d9..65093316a4 100644
--- a/wagtail/documents/tests/test_models.py
+++ b/wagtail/documents/tests/test_models.py
@@ -217,8 +217,12 @@ class TestDocumentValidateExtensions(TestCase):
         creation when called full_clean. This specific testcase invalid
         file extension is passed
         """
-        with self.assertRaises(ValidationError):
+        with self.assertRaises(ValidationError) as cm:
             self.document_invalid.full_clean()
+        expected_message = (
+            "File extension “doc” is not allowed. Allowed extensions are: pdf."
+        )
+        self.assertEqual(cm.exception.message_dict["file"][0], expected_message)
 
     def test_create_doc_valid_extension(self):
         """