diff --git a/jupyterhub/handlers/base.py b/jupyterhub/handlers/base.py
index e5764f3b..0db1660c 100644
--- a/jupyterhub/handlers/base.py
+++ b/jupyterhub/handlers/base.py
@@ -40,6 +40,7 @@ from ..metrics import SERVER_STOP_DURATION_SECONDS
 from ..metrics import ServerPollStatus
 from ..metrics import ServerSpawnStatus
 from ..metrics import ServerStopStatus
+from ..metrics import TOTAL_USERS
 from ..objects import Server
 from ..spawner import LocalProcessSpawner
 from ..user import User
@@ -453,6 +454,7 @@ class BaseHandler(RequestHandler):
             # not found, create and register user
             u = orm.User(name=username)
             self.db.add(u)
+            TOTAL_USERS.inc()
             self.db.commit()
             user = self._user_from_orm(u)
         return user
diff --git a/jupyterhub/tests/mocking.py b/jupyterhub/tests/mocking.py
index 4cadd128..5ae6ec8c 100644
--- a/jupyterhub/tests/mocking.py
+++ b/jupyterhub/tests/mocking.py
@@ -41,6 +41,7 @@ from traitlets import Bool
 from traitlets import default
 from traitlets import Dict
 
+from .. import metrics
 from .. import orm
 from ..app import JupyterHub
 from ..auth import PAMAuthenticator
@@ -327,6 +328,7 @@ class MockHub(JupyterHub):
             user = orm.User(name='user')
             self.db.add(user)
             self.db.commit()
+            metrics.TOTAL_USERS.inc()
 
     def stop(self):
         super().stop()
diff --git a/jupyterhub/tests/test_metrics.py b/jupyterhub/tests/test_metrics.py
new file mode 100644
index 00000000..29c22122
--- /dev/null
+++ b/jupyterhub/tests/test_metrics.py
@@ -0,0 +1,34 @@
+import json
+
+from .utils import add_user
+from .utils import api_request
+from jupyterhub import metrics
+from jupyterhub import orm
+
+
+async def test_total_users(app):
+    num_users = app.db.query(orm.User).count()
+    sample = metrics.TOTAL_USERS.collect()[0].samples[0]
+    assert sample.value == num_users
+
+    await api_request(
+        app, "/users", method="post", data=json.dumps({"usernames": ["incrementor"]})
+    )
+
+    sample = metrics.TOTAL_USERS.collect()[0].samples[0]
+    assert sample.value == num_users + 1
+
+    # GET /users used to double-count
+    await api_request(app, "/users")
+
+    # populate the Users cache dict if any are missing:
+    for user in app.db.query(orm.User):
+        _ = app.users[user.id]
+
+    sample = metrics.TOTAL_USERS.collect()[0].samples[0]
+    assert sample.value == num_users + 1
+
+    await api_request(app, "/users/incrementor", method="delete")
+
+    sample = metrics.TOTAL_USERS.collect()[0].samples[0]
+    assert sample.value == num_users
diff --git a/jupyterhub/tests/utils.py b/jupyterhub/tests/utils.py
index 09aeb196..fd69178f 100644
--- a/jupyterhub/tests/utils.py
+++ b/jupyterhub/tests/utils.py
@@ -4,6 +4,7 @@ from concurrent.futures import ThreadPoolExecutor
 import requests
 from certipy import Certipy
 
+from jupyterhub import metrics
 from jupyterhub import orm
 from jupyterhub.objects import Server
 from jupyterhub.utils import url_path_join as ujoin
@@ -97,6 +98,7 @@ def add_user(db, app=None, **kwargs):
     if orm_user is None:
         orm_user = orm.User(**kwargs)
         db.add(orm_user)
+        metrics.TOTAL_USERS.inc()
     else:
         for attr, value in kwargs.items():
             setattr(orm_user, attr, value)
diff --git a/jupyterhub/user.py b/jupyterhub/user.py
index a970c120..bf8603f8 100644
--- a/jupyterhub/user.py
+++ b/jupyterhub/user.py
@@ -69,7 +69,6 @@ class UserDict(dict):
         """Add a user to the UserDict"""
         if orm_user.id not in self:
             self[orm_user.id] = self.from_orm(orm_user)
-            TOTAL_USERS.inc()
         return self[orm_user.id]
 
     def __contains__(self, key):