diff --git a/rest_framework/serializers.py b/rest_framework/serializers.py
index b4026852c..21336dc29 100644
--- a/rest_framework/serializers.py
+++ b/rest_framework/serializers.py
@@ -26,13 +26,17 @@ class NestedValidationError(ValidationError):
     if the messages are a list of error messages.
 
     In the case of nested serializers, where the parent has many children,
-    then the child's `serializer.errors` will be a list of dicts.
+    then the child's `serializer.errors` will be a list of dicts.  In the case
+    of a single child, the `serializer.errors` will be a dict.
 
     We need to override the default behavior to get properly nested error dicts.
     """
 
     def __init__(self, message):
-        self.messages = message
+        if isinstance(message, dict):
+            self.messages = [message]
+        else:
+            self.messages = message
 
 
 class DictWithMetadata(dict):
@@ -311,8 +315,8 @@ class BaseSerializer(WritableField):
 
     def field_to_native(self, obj, field_name):
         """
-        Override default so that we can apply ModelSerializer as a nested
-        field to relationships.
+        Override default so that the serializer can be used as a nested field
+        across relationships.
         """
         if self.source == '*':
             return self.to_native(obj)
@@ -344,6 +348,10 @@ class BaseSerializer(WritableField):
         return self.to_native(value)
 
     def field_from_native(self, data, files, field_name, into):
+        """
+        Override default so that the serializer can be used as a writable
+        nested field across relationships.
+        """
         if self.read_only:
             return
 
@@ -354,15 +362,14 @@ class BaseSerializer(WritableField):
                 raise ValidationError(self.error_messages['required'])
             return
 
-        if self.parent.object:
-            # Set the serializer object if it exists
-            obj = getattr(self.parent.object, field_name)
-            self.object = obj
+        # Set the serializer object if it exists
+        obj = getattr(self.parent.object, field_name) if self.parent.object else None
 
         if value in (None, ''):
             into[(self.source or field_name)] = None
         else:
             kwargs = {
+                'instance': obj,
                 'data': value,
                 'context': self.context,
                 'partial': self.partial,
@@ -371,7 +378,6 @@ class BaseSerializer(WritableField):
             serializer = self.__class__(**kwargs)
 
             if serializer.is_valid():
-                self.object = serializer.object
                 into[self.source or field_name] = serializer.object
             else:
                 # Propagate errors up to our parent
@@ -630,33 +636,43 @@ class ModelSerializer(Serializer):
         """
         Restore the model instance.
         """
-        self.m2m_data = {}
-        self.related_data = {}
+        m2m_data = {}
+        related_data = {}
+        meta = self.opts.model._meta
 
-        # Reverse fk relations
-        for (obj, model) in self.opts.model._meta.get_all_related_objects_with_model():
+        # Reverse fk or one-to-one relations
+        for (obj, model) in meta.get_all_related_objects_with_model():
             field_name = obj.field.related_query_name()
             if field_name in attrs:
-                self.related_data[field_name] = attrs.pop(field_name)
+                related_data[field_name] = attrs.pop(field_name)
 
         # Reverse m2m relations
-        for (obj, model) in self.opts.model._meta.get_all_related_m2m_objects_with_model():
+        for (obj, model) in meta.get_all_related_m2m_objects_with_model():
             field_name = obj.field.related_query_name()
             if field_name in attrs:
-                self.m2m_data[field_name] = attrs.pop(field_name)
+                m2m_data[field_name] = attrs.pop(field_name)
 
         # Forward m2m relations
-        for field in self.opts.model._meta.many_to_many:
+        for field in meta.many_to_many:
             if field.name in attrs:
-                self.m2m_data[field.name] = attrs.pop(field.name)
+                m2m_data[field.name] = attrs.pop(field.name)
 
+        # Update an existing instance...
         if instance is not None:
             for key, val in attrs.items():
                 setattr(instance, key, val)
 
+        # ...or create a new instance
         else:
             instance = self.opts.model(**attrs)
 
+        # Any relations that cannot be set until we've
+        # saved the model get hidden away on these
+        # private attributes, so we can deal with them
+        # at the point of save.
+        instance._related_data = related_data
+        instance._m2m_data = m2m_data
+
         return instance
 
     def from_native(self, data, files):
@@ -673,15 +689,24 @@ class ModelSerializer(Serializer):
         """
         obj.save(**kwargs)
 
-        if getattr(self, 'm2m_data', None):
-            for accessor_name, object_list in self.m2m_data.items():
-                setattr(self.object, accessor_name, object_list)
-            self.m2m_data = {}
+        if getattr(obj, '_m2m_data', None):
+            for accessor_name, object_list in obj._m2m_data.items():
+                setattr(obj, accessor_name, object_list)
+            del(obj._m2m_data)
 
-        if getattr(self, 'related_data', None):
-            for accessor_name, object_list in self.related_data.items():
-                setattr(self.object, accessor_name, object_list)
-            self.related_data = {}
+        if getattr(obj, '_related_data', None):
+            for accessor_name, related in obj._related_data.items():
+                if related is None:
+                    previous = getattr(obj, accessor_name, related)
+                    if previous:
+                        previous.delete()
+                elif isinstance(related, models.Model):
+                    fk_field = obj._meta.get_field_by_name(accessor_name)[0].field.name
+                    setattr(related, fk_field, obj)
+                    self.save_object(related)
+                else:
+                    setattr(obj, accessor_name, related)
+            del(obj._related_data)
 
 
 class HyperlinkedModelSerializerOptions(ModelSerializerOptions):
diff --git a/rest_framework/tests/relations_nested.py b/rest_framework/tests/relations_nested.py
index a125ba656..4592e5593 100644
--- a/rest_framework/tests/relations_nested.py
+++ b/rest_framework/tests/relations_nested.py
@@ -1,115 +1,125 @@
 from __future__ import unicode_literals
+from django.db import models
 from django.test import TestCase
 from rest_framework import serializers
-from rest_framework.tests.models import ForeignKeyTarget, ForeignKeySource, NullableForeignKeySource, OneToOneTarget, NullableOneToOneSource
 
 
-class ForeignKeySourceSerializer(serializers.ModelSerializer):
+class OneToOneTarget(models.Model):
+    name = models.CharField(max_length=100)
+
+
+class OneToOneTargetSource(models.Model):
+    name = models.CharField(max_length=100)
+    target = models.OneToOneField(OneToOneTarget, null=True, blank=True,
+                                  related_name='target_source')
+
+
+class OneToOneSource(models.Model):
+    name = models.CharField(max_length=100)
+    target_source = models.OneToOneField(OneToOneTargetSource, related_name='source')
+
+
+class OneToOneSourceSerializer(serializers.ModelSerializer):
     class Meta:
-        depth = 1
-        model = ForeignKeySource
+        model = OneToOneSource
+        exclude = ('target_source', )
 
 
-class FlatForeignKeySourceSerializer(serializers.ModelSerializer):
-    class Meta:
-        model = ForeignKeySource
-
-
-class ForeignKeyTargetSerializer(serializers.ModelSerializer):
-    sources = FlatForeignKeySourceSerializer(many=True)
+class OneToOneTargetSourceSerializer(serializers.ModelSerializer):
+    source = OneToOneSourceSerializer()
 
     class Meta:
-        model = ForeignKeyTarget
+        model = OneToOneTargetSource
+        exclude = ('target', )
 
 
-class NullableForeignKeySourceSerializer(serializers.ModelSerializer):
-    class Meta:
-        depth = 1
-        model = NullableForeignKeySource
-
-
-class NullableOneToOneSourceSerializer(serializers.ModelSerializer):
-    class Meta:
-        model = NullableOneToOneSource
-
-
-class NullableOneToOneTargetSerializer(serializers.ModelSerializer):
-    nullable_source = NullableOneToOneSourceSerializer()
+class OneToOneTargetSerializer(serializers.ModelSerializer):
+    target_source = OneToOneTargetSourceSerializer()
 
     class Meta:
         model = OneToOneTarget
 
 
-class ReverseForeignKeyTests(TestCase):
+class NestedOneToOneTests(TestCase):
     def setUp(self):
-        target = ForeignKeyTarget(name='target-1')
-        target.save()
-        new_target = ForeignKeyTarget(name='target-2')
-        new_target.save()
         for idx in range(1, 4):
-            source = ForeignKeySource(name='source-%d' % idx, target=target)
+            target = OneToOneTarget(name='target-%d' % idx)
+            target.save()
+            target_source = OneToOneTargetSource(name='target-source-%d' % idx, target=target)
+            target_source.save()
+            source = OneToOneSource(name='source-%d' % idx, target_source=target_source)
             source.save()
 
-    def test_foreign_key_retrieve(self):
-        queryset = ForeignKeySource.objects.all()
-        serializer = ForeignKeySourceSerializer(queryset, many=True)
-        expected = [
-            {'id': 1, 'name': 'source-1', 'target': {'id': 1, 'name': 'target-1'}},
-            {'id': 2, 'name': 'source-2', 'target': {'id': 1, 'name': 'target-1'}},
-            {'id': 3, 'name': 'source-3', 'target': {'id': 1, 'name': 'target-1'}},
-        ]
-        self.assertEqual(serializer.data, expected)
-
-    def test_reverse_foreign_key_retrieve(self):
-        queryset = ForeignKeyTarget.objects.all()
-        serializer = ForeignKeyTargetSerializer(queryset, many=True)
-        expected = [
-            {'id': 1, 'name': 'target-1', 'sources': [
-                {'id': 1, 'name': 'source-1', 'target': 1},
-                {'id': 2, 'name': 'source-2', 'target': 1},
-                {'id': 3, 'name': 'source-3', 'target': 1},
-            ]},
-            {'id': 2, 'name': 'target-2', 'sources': [
-            ]}
-        ]
-        self.assertEqual(serializer.data, expected)
-
-
-class NestedNullableForeignKeyTests(TestCase):
-    def setUp(self):
-        target = ForeignKeyTarget(name='target-1')
-        target.save()
-        for idx in range(1, 4):
-            if idx == 3:
-                target = None
-            source = NullableForeignKeySource(name='source-%d' % idx, target=target)
-            source.save()
-
-    def test_foreign_key_retrieve_with_null(self):
-        queryset = NullableForeignKeySource.objects.all()
-        serializer = NullableForeignKeySourceSerializer(queryset, many=True)
-        expected = [
-            {'id': 1, 'name': 'source-1', 'target': {'id': 1, 'name': 'target-1'}},
-            {'id': 2, 'name': 'source-2', 'target': {'id': 1, 'name': 'target-1'}},
-            {'id': 3, 'name': 'source-3', 'target': None},
-        ]
-        self.assertEqual(serializer.data, expected)
-
-
-class NestedNullableOneToOneTests(TestCase):
-    def setUp(self):
-        target = OneToOneTarget(name='target-1')
-        target.save()
-        new_target = OneToOneTarget(name='target-2')
-        new_target.save()
-        source = NullableOneToOneSource(name='source-1', target=target)
-        source.save()
-
-    def test_reverse_foreign_key_retrieve_with_null(self):
+    def test_one_to_one_retrieve(self):
         queryset = OneToOneTarget.objects.all()
-        serializer = NullableOneToOneTargetSerializer(queryset, many=True)
+        serializer = OneToOneTargetSerializer(queryset)
         expected = [
-            {'id': 1, 'name': 'target-1', 'nullable_source': {'id': 1, 'name': 'source-1', 'target': 1}},
-            {'id': 2, 'name': 'target-2', 'nullable_source': None},
+            {'id': 1, 'name': 'target-1', 'target_source': {'id': 1, 'name': 'target-source-1', 'source': {'id': 1, 'name': 'source-1'}}},
+            {'id': 2, 'name': 'target-2', 'target_source': {'id': 2, 'name': 'target-source-2', 'source': {'id': 2, 'name': 'source-2'}}},
+            {'id': 3, 'name': 'target-3', 'target_source': {'id': 3, 'name': 'target-source-3', 'source': {'id': 3, 'name': 'source-3'}}}
+        ]
+        self.assertEqual(serializer.data, expected)
+
+    def test_one_to_one_create(self):
+        data = {'id': 4, 'name': 'target-4', 'target_source': {'id': 4, 'name': 'target-source-4', 'source': {'id': 4, 'name': 'source-4'}}}
+        serializer = OneToOneTargetSerializer(data=data)
+        self.assertTrue(serializer.is_valid())
+        obj = serializer.save()
+        self.assertEqual(serializer.data, data)
+        self.assertEqual(obj.name, 'target-4')
+
+        # Ensure (target 4, target_source 4, source 4) are added, and
+        # everything else is as expected.
+        queryset = OneToOneTarget.objects.all()
+        serializer = OneToOneTargetSerializer(queryset)
+        expected = [
+            {'id': 1, 'name': 'target-1', 'target_source': {'id': 1, 'name': 'target-source-1', 'source': {'id': 1, 'name': 'source-1'}}},
+            {'id': 2, 'name': 'target-2', 'target_source': {'id': 2, 'name': 'target-source-2', 'source': {'id': 2, 'name': 'source-2'}}},
+            {'id': 3, 'name': 'target-3', 'target_source': {'id': 3, 'name': 'target-source-3', 'source': {'id': 3, 'name': 'source-3'}}},
+            {'id': 4, 'name': 'target-4', 'target_source': {'id': 4, 'name': 'target-source-4', 'source': {'id': 4, 'name': 'source-4'}}}
+        ]
+        self.assertEqual(serializer.data, expected)
+
+    def test_one_to_one_create_with_invalid_data(self):
+        data = {'id': 4, 'name': 'target-4', 'target_source': {'id': 4, 'name': 'target-source-4', 'source': {'id': 4}}}
+        serializer = OneToOneTargetSerializer(data=data)
+        self.assertFalse(serializer.is_valid())
+        self.assertEqual(serializer.errors, {'target_source': [{'source': [{'name': ['This field is required.']}]}]})
+
+    def test_one_to_one_update(self):
+        data = {'id': 3, 'name': 'target-3-updated', 'target_source': {'id': 3, 'name': 'target-source-3-updated', 'source': {'id': 3, 'name': 'source-3-updated'}}}
+        instance = OneToOneTarget.objects.get(pk=3)
+        serializer = OneToOneTargetSerializer(instance, data=data)
+        self.assertTrue(serializer.is_valid())
+        obj = serializer.save()
+        self.assertEqual(serializer.data, data)
+        self.assertEqual(obj.name, 'target-3-updated')
+
+        # Ensure (target 3, target_source 3, source 3) are updated,
+        # and everything else is as expected.
+        queryset = OneToOneTarget.objects.all()
+        serializer = OneToOneTargetSerializer(queryset)
+        expected = [
+            {'id': 1, 'name': 'target-1', 'target_source': {'id': 1, 'name': 'target-source-1', 'source': {'id': 1, 'name': 'source-1'}}},
+            {'id': 2, 'name': 'target-2', 'target_source': {'id': 2, 'name': 'target-source-2', 'source': {'id': 2, 'name': 'source-2'}}},
+            {'id': 3, 'name': 'target-3-updated', 'target_source': {'id': 3, 'name': 'target-source-3-updated', 'source': {'id': 3, 'name': 'source-3-updated'}}}
+        ]
+        self.assertEqual(serializer.data, expected)
+
+    def test_one_to_one_delete(self):
+        data = {'id': 3, 'name': 'target-3', 'target_source': None}
+        instance = OneToOneTarget.objects.get(pk=3)
+        serializer = OneToOneTargetSerializer(instance, data=data)
+        self.assertTrue(serializer.is_valid())
+        serializer.save()
+
+        # Ensure (target_source 3, source 3) are deleted,
+        # and everything else is as expected.
+        queryset = OneToOneTarget.objects.all()
+        serializer = OneToOneTargetSerializer(queryset)
+        expected = [
+            {'id': 1, 'name': 'target-1', 'target_source': {'id': 1, 'name': 'target-source-1', 'source': {'id': 1, 'name': 'source-1'}}},
+            {'id': 2, 'name': 'target-2', 'target_source': {'id': 2, 'name': 'target-source-2', 'source': {'id': 2, 'name': 'source-2'}}},
+            {'id': 3, 'name': 'target-3', 'target_source': None}
         ]
         self.assertEqual(serializer.data, expected)
diff --git a/rest_framework/tests/serializer_nested.py b/rest_framework/tests/serializer_nested.py
index fcf644c75..6a29c6523 100644
--- a/rest_framework/tests/serializer_nested.py
+++ b/rest_framework/tests/serializer_nested.py
@@ -1,5 +1,7 @@
 """
 Tests to cover nested serializers.
+
+Doesn't cover model serializers.
 """
 from __future__ import unicode_literals
 from django.test import TestCase
@@ -124,7 +126,7 @@ class WritableNestedSerializerObjectTests(TestCase):
             def __init__(self, order, title, duration):
                 self.order, self.title, self.duration = order, title, duration
 
-            def __cmp__(self, other):
+            def __eq__(self, other):
                 return (
                     self.order == other.order and
                     self.title == other.title and
@@ -135,7 +137,7 @@ class WritableNestedSerializerObjectTests(TestCase):
             def __init__(self, album_name, artist, tracks):
                 self.album_name, self.artist, self.tracks = album_name, artist, tracks
 
-            def __cmp__(self, other):
+            def __eq__(self, other):
                 return (
                     self.album_name == other.album_name and
                     self.artist == other.artist and