diff --git a/rest_framework/serializers.py b/rest_framework/serializers.py
index 3e33f7867..78a3020ea 100644
--- a/rest_framework/serializers.py
+++ b/rest_framework/serializers.py
@@ -622,6 +622,7 @@ class ModelSerializerOptions(SerializerOptions):
         self.model = getattr(meta, 'model', None)
         self.read_only_fields = getattr(meta, 'read_only_fields', ())
         self.write_only_fields = getattr(meta, 'write_only_fields', ())
+        self.use_model_error_messages = getattr(meta, 'use_model_error_messages', False)
 
 
 class ModelSerializer(Serializer):
@@ -782,7 +783,7 @@ class ModelSerializer(Serializer):
                 "Non-existant field '%s' specified in `write_only_fields` "
                 "on serializer '%s'." %
                 (field_name, self.__class__.__name__))
-            ret[field_name].write_only = True            
+            ret[field_name].write_only = True
 
         return ret
 
@@ -848,7 +849,7 @@ class ModelSerializer(Serializer):
         if model_field.help_text is not None:
             kwargs['help_text'] = model_field.help_text
 
-        if model_field.error_messages is not None:
+        if self.opts.use_model_error_messages and model_field.error_messages is not None:
             kwargs['error_messages'] = model_field.error_messages
 
         # TODO: TypedChoiceField?
diff --git a/rest_framework/tests/test_serializer.py b/rest_framework/tests/test_serializer.py
index a1e3601f9..f1bf2a72c 100644
--- a/rest_framework/tests/test_serializer.py
+++ b/rest_framework/tests/test_serializer.py
@@ -1842,35 +1842,51 @@ class BoolenFieldTypeTest(TestCase):
         self.assertEqual(type(bfield), fields.BooleanField)
 
 
-class ErrorMessagesOnAutogeneratedFieldsTests(TestCase):
+class ModelErrorMessagesFieldsTests(TestCase):
 
     def setUp(self):
-        class EMOAFModel(RESTFrameworkModel):
+        class ErrorMessageModel(RESTFrameworkModel):
             char_field = models.CharField(blank=False, max_length=5, error_messages={
-                'required': 'required',
                 'max_length': 'max_length %(limit_value)d',
             })
+            int_field = models.IntegerField({
+                'required': 'int required model',
+                'invalid': 'int invalid',
+            })
+
+        class ErrorMessageSerializer(serializers.ModelSerializer):
+            int_field = serializers.IntegerField(error_messages={
+                'required': 'int required',
+            })
 
-        class EMOAFSerializer(serializers.ModelSerializer):
             class Meta:
-                model = EMOAFModel
+                model = ErrorMessageModel
 
-        self.serializer_class = EMOAFSerializer
+        self.serializer_class = ErrorMessageSerializer
+
+    def error_test(self, data, expected_error_field, expected_message, enabled=False):
+        self.serializer_class.Meta.use_model_error_messages = enabled
 
-    def error_test(self, data, expected_message):
         serializer = self.serializer_class(data=data)
         self.assertEqual(serializer.is_valid(), False)
         self.assertEqual(len(serializer.errors), 1)
 
         for (field_name, message) in serializer.errors.items():
-            self.assertEqual('char_field', field_name)
+            self.assertEqual(expected_error_field, field_name)
             self.assertEqual(expected_message, message[0])
 
-    def test_required(self):
-        self.error_test({}, 'required')
+    def test_model_field_required(self):
+        self.error_test({'int_field': 10, 'char_field': None}, 'char_field', 'This field is required.', enabled=True)
+        self.error_test({'int_field': 10, 'char_field': None}, 'char_field', 'This field is required.', enabled=False)
 
-    def test_required(self):
-        self.error_test({'char_field': None}, 'required')
+    def test_model_field_validation_failure(self):
+        self.error_test({'int_field': 10, 'char_field': 'abcdef'}, 'char_field', 'max_length 5', enabled=True)
+        self.error_test({'int_field': 10, 'char_field': 'abcdef'}, 'char_field', 'Ensure this value has at most 5 characters (it has 6).', enabled=False)
 
-    def test_max_length(self):
-        self.error_test({'char_field': 'abcdef'}, 'max_length 5')
+    def test_serializer_field_required(self):
+        self.error_test({'char_field': 'abcde'}, 'int_field', 'int required', enabled=True)
+        self.error_test({'char_field': 'abcde'}, 'int_field', 'int required', enabled=False)
+
+    def test_serializer_field_validation_failure(self):
+        self.error_test({'int_field': 'abc', 'char_field': 'abcde'}, 'int_field', 'Enter a whole number.', enabled=True)
+        self.error_test({'int_field': 'abc', 'char_field': 'abcde'}, 'int_field', 'Enter a whole number.', enabled=False)