diff --git a/src/api-service/__app__/onefuzzlib/proxy.py b/src/api-service/__app__/onefuzzlib/proxy.py
index dd2e6196b..5e58ab3cc 100644
--- a/src/api-service/__app__/onefuzzlib/proxy.py
+++ b/src/api-service/__app__/onefuzzlib/proxy.py
@@ -169,6 +169,9 @@ class Proxy(ORMMixin):
         self.delete()
 
     def is_outdated(self) -> bool:
+        if self.state not in VmState.available():
+            return True
+
         if self.version != __version__:
             logging.info(
                 PROXY_LOG_PREFIX + "mismatch version: proxy:%s service:%s state:%s",
diff --git a/src/api-service/__app__/timer_daily/__init__.py b/src/api-service/__app__/timer_daily/__init__.py
index 7f182fbe3..15b338e44 100644
--- a/src/api-service/__app__/timer_daily/__init__.py
+++ b/src/api-service/__app__/timer_daily/__init__.py
@@ -6,43 +6,13 @@
 import logging
 
 import azure.functions as func
-from onefuzztypes.enums import VmState
-from onefuzztypes.events import EventProxyCreated
 
-from ..onefuzzlib.events import get_events, send_event
-from ..onefuzzlib.proxy import Proxy
+from ..onefuzzlib.events import get_events
 from ..onefuzzlib.webhooks import WebhookMessageLog
 from ..onefuzzlib.workers.scalesets import Scaleset
 
 
 def main(mytimer: func.TimerRequest, dashboard: func.Out[str]) -> None:  # noqa: F841
-    proxy_list = Proxy.search()
-    # Marking Outdated Proxies. Subsequently, shutting down Outdated & Unused Proxies.
-    for proxy in proxy_list:
-        if proxy.is_outdated():
-            logging.info("marking proxy in %s as outdated.", proxy.region)
-            proxy.outdated = True
-            proxy.save()
-    # Creating a new proxy if no proxy exists for a given region.
-    for proxy in proxy_list:
-        if proxy.outdated:
-            region_list = list(
-                filter(
-                    lambda x: (x.region == proxy.region and not x.outdated),
-                    proxy_list,
-                )
-            )
-            if not len(region_list):
-                logging.info("outdated proxy in %s, creating new one.", proxy.region)
-                new_proxy = Proxy(region=proxy.region)
-                new_proxy.save()
-                send_event(
-                    EventProxyCreated(region=proxy.region, proxy_id=proxy.proxy_id)
-                )
-            if not proxy.is_used():
-                logging.info("stopping one proxy in %s.", proxy.region)
-                proxy.set_state(VmState.stopping)
-
     scalesets = Scaleset.search()
     for scaleset in scalesets:
         logging.info("updating scaleset configs: %s", scaleset.scaleset_id)
diff --git a/src/api-service/__app__/timer_proxy/__init__.py b/src/api-service/__app__/timer_proxy/__init__.py
index 7d5f03a09..22a2dbd74 100644
--- a/src/api-service/__app__/timer_proxy/__init__.py
+++ b/src/api-service/__app__/timer_proxy/__init__.py
@@ -11,20 +11,27 @@ from onefuzztypes.enums import VmState
 from ..onefuzzlib.events import get_events
 from ..onefuzzlib.orm import process_state_updates
 from ..onefuzzlib.proxy import PROXY_LOG_PREFIX, Proxy
+from ..onefuzzlib.workers.scalesets import Scaleset
 
 
 def main(mytimer: func.TimerRequest, dashboard: func.Out[str]) -> None:  # noqa: F841
-    # Reminder, proxies are created on-demand.  If something is "wrong" with
-    # a proxy, the plan is: delete and recreate it.
-    for proxy in Proxy.search():
-        if not proxy.is_alive():
-            logging.error(
-                PROXY_LOG_PREFIX + "alive check failed, stopping: %s", proxy.region
-            )
-            proxy.set_state(VmState.stopping)
-            proxy.save()
-        else:
-            proxy.save_proxy_config()
+    proxies = Proxy.search()
+    for proxy in proxies:
+        if proxy.state in VmState.available():
+            # Note, outdated checked at the start, but set at the end of this loop.
+            # As this function is called via a timer, this works around a user
+            # requesting to use the proxy while this function is checking if it's
+            # out of date
+            if proxy.outdated and not proxy.is_used():
+                proxy.set_state(VmState.stopping)
+            # If something is "wrong" with a proxy, delete & recreate it
+            elif not proxy.is_alive():
+                logging.error(
+                    PROXY_LOG_PREFIX + "alive check failed, stopping: %s", proxy.region
+                )
+                proxy.set_state(VmState.stopping)
+            else:
+                proxy.save_proxy_config()
 
         if proxy.state in VmState.needs_work():
             logging.info(
@@ -34,6 +41,17 @@ def main(mytimer: func.TimerRequest, dashboard: func.Out[str]) -> None:  # noqa:
             )
             process_state_updates(proxy)
 
+        if proxy.is_outdated():
+            proxy.outdated = True
+            proxy.save()
+
+    # make sure there is a proxy for every currently active region
+    scalesets = Scaleset.search()
+    regions = set(x.region for x in scalesets)
+    for region in regions:
+        if all(x.outdated for x in proxies if x.region == region):
+            Proxy.get_or_create(region)
+
     events = get_events()
     if events:
         dashboard.set(events)