diff --git a/pageserver/src/http/openapi_spec.yml b/pageserver/src/http/openapi_spec.yml
index 50614653be..33a2e32141 100644
--- a/pageserver/src/http/openapi_spec.yml
+++ b/pageserver/src/http/openapi_spec.yml
@@ -186,10 +186,8 @@ paths:
               schema:
                 $ref: "#/components/schemas/Error"
     delete:
-      description: "Attempts to delete specified timeline. On 500 errors should be retried"
+      description: "Attempts to delete specified timeline. 500 and 409 errors should be retried"
       responses:
-        "200":
-          description: Ok
         "400":
           description: Error when no tenant id found in path or no timeline id
           content:
@@ -214,6 +212,12 @@ paths:
             application/json:
               schema:
                 $ref: "#/components/schemas/NotFoundError"
+        "409":
+          description: Deletion is already in progress, continue polling
+          content:
+            application/json:
+              schema:
+                $ref: "#/components/schemas/ConflictError"
         "412":
           description: Tenant is missing, or timeline has children
           content:
diff --git a/pageserver/src/http/routes.rs b/pageserver/src/http/routes.rs
index 8d3bb5552b..0e12cc2b1e 100644
--- a/pageserver/src/http/routes.rs
+++ b/pageserver/src/http/routes.rs
@@ -187,6 +187,7 @@ impl From<crate::tenant::DeleteTimelineError> for ApiError {
                 format!("Cannot delete timeline which has child timelines: {children:?}")
                     .into_boxed_str(),
             ),
+            a @ AlreadyInProgress => ApiError::Conflict(a.to_string()),
             Other(e) => ApiError::InternalServerError(e),
         }
     }
diff --git a/pageserver/src/tenant.rs b/pageserver/src/tenant.rs
index 0e8d6b1287..ce1e5bf51f 100644
--- a/pageserver/src/tenant.rs
+++ b/pageserver/src/tenant.rs
@@ -440,8 +440,13 @@ pub enum GetTimelineError {
 pub enum DeleteTimelineError {
     #[error("NotFound")]
     NotFound,
+
     #[error("HasChildren")]
     HasChildren(Vec<TimelineId>),
+
+    #[error("Timeline deletion is already in progress")]
+    AlreadyInProgress,
+
     #[error(transparent)]
     Other(#[from] anyhow::Error),
 }
@@ -1755,14 +1760,11 @@ impl Tenant {
             timeline = Arc::clone(timeline_entry.get());
 
             // Prevent two tasks from trying to delete the timeline at the same time.
-            delete_lock_guard =
-                DeletionGuard(Arc::clone(&timeline.delete_lock).try_lock_owned().map_err(
-                    |_| {
-                        DeleteTimelineError::Other(anyhow::anyhow!(
-                            "timeline deletion is already in progress"
-                        ))
-                    },
-                )?);
+            delete_lock_guard = DeletionGuard(
+                Arc::clone(&timeline.delete_lock)
+                    .try_lock_owned()
+                    .map_err(|_| DeleteTimelineError::AlreadyInProgress)?,
+            );
 
             // If another task finished the deletion just before we acquired the lock,
             // return success.
diff --git a/test_runner/regress/test_timeline_delete.py b/test_runner/regress/test_timeline_delete.py
index ddd9ffd755..7c3424cf32 100644
--- a/test_runner/regress/test_timeline_delete.py
+++ b/test_runner/regress/test_timeline_delete.py
@@ -463,10 +463,10 @@ def test_concurrent_timeline_delete_stuck_on(
 
         # make the second call and assert behavior
         log.info("second call start")
-        error_msg_re = "timeline deletion is already in progress"
+        error_msg_re = "Timeline deletion is already in progress"
         with pytest.raises(PageserverApiException, match=error_msg_re) as second_call_err:
             ps_http.timeline_delete(env.initial_tenant, child_timeline_id)
-        assert second_call_err.value.status_code == 500
+        assert second_call_err.value.status_code == 409
         env.pageserver.allowed_errors.append(f".*{child_timeline_id}.*{error_msg_re}.*")
         # the second call will try to transition the timeline into Stopping state as well
         env.pageserver.allowed_errors.append(
@@ -518,9 +518,9 @@ def test_delete_timeline_client_hangup(neon_env_builder: NeonEnvBuilder):
         ps_http.timeline_delete(env.initial_tenant, child_timeline_id, timeout=2)
 
     env.pageserver.allowed_errors.append(
-        f".*{child_timeline_id}.*timeline deletion is already in progress.*"
+        f".*{child_timeline_id}.*Timeline deletion is already in progress.*"
     )
-    with pytest.raises(PageserverApiException, match="timeline deletion is already in progress"):
+    with pytest.raises(PageserverApiException, match="Timeline deletion is already in progress"):
         ps_http.timeline_delete(env.initial_tenant, child_timeline_id, timeout=2)
 
     # make sure the timeout was due to the failpoint