diff --git a/src/sentry/hybridcloud/services/control_organization_provisioning/impl.py b/src/sentry/hybridcloud/services/control_organization_provisioning/impl.py
index 0df1b35184b499..9253658e48cc0f 100644
--- a/src/sentry/hybridcloud/services/control_organization_provisioning/impl.py
+++ b/src/sentry/hybridcloud/services/control_organization_provisioning/impl.py
@@ -1,6 +1,6 @@
 from copy import deepcopy
 
-from django.db import router, transaction
+from django.db import IntegrityError, router, transaction
 from django.utils import timezone as django_timezone
 
 from sentry import features, roles
@@ -188,7 +188,7 @@ def update_organization_slug(
         organization_id: int,
         desired_slug: str,
         require_exact: bool = True,
-    ) -> RpcOrganizationSlugReservation:
+    ) -> RpcOrganizationSlugReservation | None:
         existing_slug_reservations = list(
             OrganizationSlugReservation.objects.filter(organization_id=organization_id)
         )
@@ -216,27 +216,34 @@ def update_organization_slug(
         if not require_exact:
             slug_base = self._generate_org_slug(region_name=region_name, slug=slug_base)
 
-        with outbox_context(
-            transaction.atomic(using=router.db_for_write(OrganizationSlugReservation))
-        ):
-            OrganizationSlugReservation(
-                slug=slug_base,
-                organization_id=organization_id,
-                user_id=-1,
-                region_name=region_name,
-                reservation_type=OrganizationSlugReservationType.TEMPORARY_RENAME_ALIAS.value,
-            ).save(unsafe_write=True)
-
-            org_mapping = OrganizationMapping.objects.filter(
-                organization_id=organization_id
-            ).first()
-            org = serialize_organization_mapping(org_mapping) if org_mapping is not None else None
-            if org and features.has("organizations:revoke-org-auth-on-slug-rename", org):
-                # Changing a slug invalidates all org tokens, so revoke them all.
-                auth_tokens = OrgAuthToken.objects.filter(
-                    organization_id=organization_id, date_deactivated__isnull=True
+        try:
+            with outbox_context(
+                transaction.atomic(using=router.db_for_write(OrganizationSlugReservation))
+            ):
+                OrganizationSlugReservation(
+                    slug=slug_base,
+                    organization_id=organization_id,
+                    user_id=-1,
+                    region_name=region_name,
+                    reservation_type=OrganizationSlugReservationType.TEMPORARY_RENAME_ALIAS.value,
+                ).save(unsafe_write=True)
+
+                org_mapping = OrganizationMapping.objects.filter(
+                    organization_id=organization_id
+                ).first()
+                org = (
+                    serialize_organization_mapping(org_mapping) if org_mapping is not None else None
                 )
-                auth_tokens.update(date_deactivated=django_timezone.now())
+                if org and features.has("organizations:revoke-org-auth-on-slug-rename", org):
+                    # Changing a slug invalidates all org tokens, so revoke them all.
+                    auth_tokens = OrgAuthToken.objects.filter(
+                        organization_id=organization_id, date_deactivated__isnull=True
+                    )
+                    auth_tokens.update(date_deactivated=django_timezone.now())
+        except IntegrityError:
+            if require_exact:
+                return None
+            raise
 
         primary_slug = self._validate_primary_slug_updated(
             organization_id=organization_id, slug_base=slug_base
diff --git a/src/sentry/hybridcloud/services/control_organization_provisioning/service.py b/src/sentry/hybridcloud/services/control_organization_provisioning/service.py
index 3b33ea075700a7..7b1f4090636def 100644
--- a/src/sentry/hybridcloud/services/control_organization_provisioning/service.py
+++ b/src/sentry/hybridcloud/services/control_organization_provisioning/service.py
@@ -57,7 +57,7 @@ def update_organization_slug(
         organization_id: int,
         desired_slug: str,
         require_exact: bool = True,
-    ) -> RpcOrganizationSlugReservation:
+    ) -> RpcOrganizationSlugReservation | None:
         """
         Updates an organization's slug via an outbox based confirmation flow to ensure that the control
         and region silos stay in sync.
@@ -71,7 +71,7 @@ def update_organization_slug(
         :param desired_slug: The slug to update the organization with
         :param require_exact: Determines whether the slug can be modified with a unique suffix in the
         case of a slug collision.
-        :return:
+        :return: The updated slug reservation, or None if require_exact=True and the slug is already taken.
         """
 
     @abstractmethod
diff --git a/src/sentry/services/organization/provisioning.py b/src/sentry/services/organization/provisioning.py
index ef6c4ab8c62bd2..4343c1894d2b34 100644
--- a/src/sentry/services/organization/provisioning.py
+++ b/src/sentry/services/organization/provisioning.py
@@ -114,6 +114,9 @@ def _control_based_slug_change(
             )
         )
 
+        if rpc_slug_reservation is None:
+            raise OrganizationSlugCollisionException
+
         rpc_org = organization_service.get(id=rpc_slug_reservation.organization_id)
 
         if rpc_org is None:
diff --git a/tests/sentry/hybridcloud/services/test_control_organization_provisioning.py b/tests/sentry/hybridcloud/services/test_control_organization_provisioning.py
index d45f6786e920ef..46cc22059f4182 100644
--- a/tests/sentry/hybridcloud/services/test_control_organization_provisioning.py
+++ b/tests/sentry/hybridcloud/services/test_control_organization_provisioning.py
@@ -1,7 +1,7 @@
 from __future__ import annotations
 
 import pytest
-from django.db import IntegrityError, router, transaction
+from django.db import router, transaction
 from django.db.models import QuerySet
 
 from sentry.hybridcloud.models.outbox import outbox_context
@@ -251,22 +251,13 @@ def test_fails_to_update_exact_slug_with_collision(self) -> None:
         self.provisioning_args.provision_options.slug = conflicting_slug
         org_with_conflicting_slug = self.provision_organization()
 
-        if SiloMode.get_current_mode() == SiloMode.REGION:
-            with pytest.raises(RpcRemoteException):
-                control_organization_provisioning_rpc_service.update_organization_slug(
-                    organization_id=test_org_slug_reservation.organization_id,
-                    desired_slug=conflicting_slug,
-                    require_exact=True,
-                    region_name=self.region_name,
-                )
-        else:
-            with pytest.raises(IntegrityError):
-                control_organization_provisioning_rpc_service.update_organization_slug(
-                    organization_id=test_org_slug_reservation.organization_id,
-                    desired_slug=conflicting_slug,
-                    require_exact=True,
-                    region_name=self.region_name,
-                )
+        result = control_organization_provisioning_rpc_service.update_organization_slug(
+            organization_id=test_org_slug_reservation.organization_id,
+            desired_slug=conflicting_slug,
+            require_exact=True,
+            region_name=self.region_name,
+        )
+        assert result is None
 
         with assume_test_silo_mode(SiloMode.CONTROL):
             org_slug_reservation = OrganizationSlugReservation.objects.get(