diff --git a/homeassistant/auth/providers/homeassistant.py b/homeassistant/auth/providers/homeassistant.py
index f5605886628..b22f93f11f1 100644
--- a/homeassistant/auth/providers/homeassistant.py
+++ b/homeassistant/auth/providers/homeassistant.py
@@ -2,7 +2,8 @@
 import base64
 from collections import OrderedDict
 import logging
-from typing import Any, Dict, List, Optional, cast
+
+from typing import Any, Dict, List, Optional, Set, cast  # noqa: F401
 
 import bcrypt
 import voluptuous as vol
@@ -52,6 +53,9 @@ class Data:
         self._store = hass.helpers.storage.Store(STORAGE_VERSION, STORAGE_KEY,
                                                  private=True)
         self._data = None  # type: Optional[Dict[str, Any]]
+        # Legacy mode will allow usernames to start/end with whitespace
+        # and will compare usernames case-insensitive.
+        # Remove in 2020 or when we launch 1.0.
         self.is_legacy = False
 
     @callback
@@ -60,7 +64,7 @@ class Data:
         if self.is_legacy:
             return username
 
-        return username.strip()
+        return username.strip().casefold()
 
     async def async_load(self) -> None:
         """Load stored data."""
@@ -71,9 +75,26 @@ class Data:
                 'users': []
             }
 
+        seen = set()  # type: Set[str]
+
         for user in data['users']:
             username = user['username']
 
+            # check if we have duplicates
+            folded = username.casefold()
+
+            if folded in seen:
+                self.is_legacy = True
+
+                logging.getLogger(__name__).warning(
+                    "Home Assistant auth provider is running in legacy mode "
+                    "because we detected usernames that are case-insensitive"
+                    "equivalent. Please change the username: '%s'.", username)
+
+                break
+
+            seen.add(folded)
+
             # check if we have unstripped usernames
             if username != username.strip():
                 self.is_legacy = True
@@ -81,7 +102,7 @@ class Data:
                 logging.getLogger(__name__).warning(
                     "Home Assistant auth provider is running in legacy mode "
                     "because we detected usernames that start or end in a "
-                    "space. Please change the username.")
+                    "space. Please change the username: '%s'.", username)
 
                 break
 
@@ -103,7 +124,7 @@ class Data:
 
         # Compare all users to avoid timing attacks.
         for user in self.users:
-            if username == user['username']:
+            if self.normalize_username(user['username']) == username:
                 found = user
 
         if found is None:
diff --git a/tests/auth/providers/test_homeassistant.py b/tests/auth/providers/test_homeassistant.py
index b654b42fb35..ffc4d67f21d 100644
--- a/tests/auth/providers/test_homeassistant.py
+++ b/tests/auth/providers/test_homeassistant.py
@@ -73,7 +73,6 @@ async def test_changing_password_raises_invalid_user(data, hass):
 async def test_adding_user(data, hass):
     """Test adding a user."""
     data.add_auth('test-user', 'test-pass')
-    data.validate_login('test-user', 'test-pass')
     data.validate_login(' test-user ', 'test-pass')
 
 
@@ -81,7 +80,7 @@ async def test_adding_user_duplicate_username(data, hass):
     """Test adding a user with duplicate username."""
     data.add_auth('test-user', 'test-pass')
     with pytest.raises(hass_auth.InvalidUser):
-        data.add_auth('test-user ', 'other-pass')
+        data.add_auth('TEST-user ', 'other-pass')
 
 
 async def test_validating_password_invalid_password(data, hass):
@@ -91,16 +90,22 @@ async def test_validating_password_invalid_password(data, hass):
     with pytest.raises(hass_auth.InvalidAuth):
         data.validate_login(' test-user ', 'invalid-pass')
 
+    with pytest.raises(hass_auth.InvalidAuth):
+        data.validate_login('test-user', 'test-pass ')
+
+    with pytest.raises(hass_auth.InvalidAuth):
+        data.validate_login('test-user', 'Test-pass')
+
 
 async def test_changing_password(data, hass):
     """Test adding a user."""
     data.add_auth('test-user', 'test-pass')
-    data.change_password('test-user ', 'new-pass')
+    data.change_password('TEST-USER ', 'new-pass')
 
     with pytest.raises(hass_auth.InvalidAuth):
         data.validate_login('test-user', 'test-pass')
 
-    data.validate_login('test-user', 'new-pass')
+    data.validate_login('test-UsEr', 'new-pass')
 
 
 async def test_login_flow_validates(data, hass):
@@ -122,18 +127,18 @@ async def test_login_flow_validates(data, hass):
     assert result['errors']['base'] == 'invalid_auth'
 
     result = await flow.async_step_init({
-        'username': 'test-user ',
+        'username': 'TEST-user ',
         'password': 'incorrect-pass',
     })
     assert result['type'] == data_entry_flow.RESULT_TYPE_FORM
     assert result['errors']['base'] == 'invalid_auth'
 
     result = await flow.async_step_init({
-        'username': 'test-user',
+        'username': 'test-USER',
         'password': 'test-pass',
     })
     assert result['type'] == data_entry_flow.RESULT_TYPE_CREATE_ENTRY
-    assert result['data']['username'] == 'test-user'
+    assert result['data']['username'] == 'test-USER'
 
 
 async def test_saving_loading(data, hass):
@@ -179,6 +184,9 @@ async def test_legacy_adding_user_duplicate_username(legacy_data, hass):
     legacy_data.add_auth('test-user', 'test-pass')
     with pytest.raises(hass_auth.InvalidUser):
         legacy_data.add_auth('test-user', 'other-pass')
+    # Not considered duplicate
+    legacy_data.add_auth('test-user ', 'test-pass')
+    legacy_data.add_auth('Test-user', 'test-pass')
 
 
 async def test_legacy_validating_password_invalid_password(legacy_data, hass):