diff --git a/zephyr/models.py b/zephyr/models.py
index 0418b112f8..a07b4bd964 100644
--- a/zephyr/models.py
+++ b/zephyr/models.py
@@ -342,25 +342,24 @@ class Message(models.Model):
 
         return bugdown.convert(content, self.sender.realm.domain, self)
 
-    def set_rendered_content(self, rendered_content):
+    def set_rendered_content(self, rendered_content, save = False):
         """Set the content on the message.
-
-        This method does not call .save(). Save afterwards with
-        update_fields=["rendered_content", "rendered_content_version"].
         """
 
         self.rendered_content = rendered_content
         self.rendered_content_version = bugdown.version
 
-        if self.rendered_content is None:
+        if self.rendered_content is not None:
+            if save:
+                self.save(update_fields=["rendered_content", "rendered_content_version"])
+            return True
+        else:
             return False
 
-        return True
-
-    def maybe_render_content(self):
+    def maybe_render_content(self, save = False):
         """Render the markdown if there is no existing rendered_content"""
-        if self.rendered_content is None:
-            return self.set_rendered_content(self.render_markdown(self.content))
+        if self.rendered_content_version < bugdown.version or self.rendered_content is None:
+            return self.set_rendered_content(self.render_markdown(self.content), save)
         else:
             return True
 
@@ -409,10 +408,9 @@ class Message(models.Model):
         if self.last_edit_time != None:
             obj['last_edit_timestamp'] = datetime_to_timestamp(self.last_edit_time)
             obj['edit_history'] = ujson.loads(self.edit_history)
-        if apply_markdown and self.rendered_content_version is not None:
-            obj['content'] = self.rendered_content
-            obj['content_type'] = 'text/html'
-        elif apply_markdown:
+
+        if apply_markdown:
+            self.maybe_render_content(save = True)
             if self.rendered_content is not None:
                 obj['content'] = self.rendered_content
             else:
diff --git a/zephyr/tests.py b/zephyr/tests.py
index b547ab503e..35668b6380 100644
--- a/zephyr/tests.py
+++ b/zephyr/tests.py
@@ -1361,6 +1361,15 @@ class GetOldMessagesTest(AuthedTestCase):
         self.exercise_bad_narrow_operand("pm-with", ['non-existent-user@humbughq.com'],
             "Invalid narrow operator: unknown user")
 
+    def test_message_without_rendered_content(self):
+        """Older messages may not have rendered_content in the database"""
+        m = Message.objects.all().order_by('-id')[0]
+        m.rendered_content = m.rendered_content_version = None
+        m.content = 'test content'
+        # Use to_dict_uncached directly to avoid having to deal with memcached
+        d = m.to_dict_uncached(True)
+        self.assertEqual(d['content'], '<p>test content</p>')
+
 class InviteUserTest(AuthedTestCase):
 
     def invite(self, users, streams):