diff --git a/pageserver/src/tenant.rs b/pageserver/src/tenant.rs
index e88dee7c6c..46317e93ee 100644
--- a/pageserver/src/tenant.rs
+++ b/pageserver/src/tenant.rs
@@ -2446,6 +2446,12 @@ impl Tenant {
             .remote_client
             .wait_completion()
             .await
+            .map_err(|e| match e {
+                WaitCompletionError::NotInitialized(
+                    e, // If the queue is already stopped, it's a shutdown error.
+                ) if e.is_stopping() => CreateTimelineError::ShuttingDown,
+                e => CreateTimelineError::Other(e.into()),
+            })
             .context("wait for timeline initial uploads to complete")?;
 
         // The creating task is responsible for activating the timeline.
diff --git a/test_runner/regress/test_tenants.py b/test_runner/regress/test_tenants.py
index 5a499ea98b..158c3fddb0 100644
--- a/test_runner/regress/test_tenants.py
+++ b/test_runner/regress/test_tenants.py
@@ -369,12 +369,16 @@ def test_create_churn_during_restart(neon_env_builder: NeonEnvBuilder):
     - Bad response codes during shutdown (e.g. returning 500 instead of 503)
     - Issues where a tenant is still starting up while we receive a request for it
     - Issues with interrupting/resuming tenant/timeline creation in shutdown
+    - Issues with a timeline is not created successfully because of restart.
     """
     env = neon_env_builder.init_configs()
     env.start()
     tenant_id: TenantId = env.initial_tenant
     timeline_id = env.initial_timeline
 
+    # At this point, the initial tenant/timeline might not have been created successfully,
+    # and this is the case we want to test.
+
     # Multiple creation requests which race will generate this error on the pageserver
     # and storage controller respectively
     env.pageserver.allowed_errors.append(".*Conflict: Tenant is already being modified.*")