diff --git a/pageserver/src/http/openapi_spec.yml b/pageserver/src/http/openapi_spec.yml
index 07712298451e..bb477f89c5bf 100644
--- a/pageserver/src/http/openapi_spec.yml
+++ b/pageserver/src/http/openapi_spec.yml
@@ -1038,7 +1038,7 @@ paths:
                   format: hex
       responses:
         "201":
-          description: TimelineInfo
+          description: Timeline was created, or already existed with matching parameters
           content:
             application/json:
               schema:
@@ -1068,11 +1068,17 @@ paths:
               schema:
                 $ref: "#/components/schemas/Error"
         "409":
-          description: Timeline already exists, creation skipped
+          description: Timeline already exists, with different parameters.  Creation cannot proceed.
           content:
             application/json:
               schema:
                 $ref: "#/components/schemas/ConflictError"
+        "429":
+          description: A creation request was sent for the same Timeline Id while a creation was already in progress.  Back off and retry.
+          content:
+            application/json:
+              schema:
+                $ref: "#/components/schemas/Error"
         "500":
           description: Generic operation error
           content:
diff --git a/pageserver/src/http/routes.rs b/pageserver/src/http/routes.rs
index 26f23fb8c2cb..3cc92216ed2a 100644
--- a/pageserver/src/http/routes.rs
+++ b/pageserver/src/http/routes.rs
@@ -535,10 +535,13 @@ async fn timeline_create_handler(
                     HttpErrorBody::from_msg("Tenant shutting down".to_string()),
                 )
             }
-            Err(
-                e @ tenant::CreateTimelineError::Conflict
-                | e @ tenant::CreateTimelineError::AlreadyCreating,
-            ) => json_response(StatusCode::CONFLICT, HttpErrorBody::from_msg(e.to_string())),
+            Err(e @ tenant::CreateTimelineError::Conflict) => {
+                json_response(StatusCode::CONFLICT, HttpErrorBody::from_msg(e.to_string()))
+            }
+            Err(e @ tenant::CreateTimelineError::AlreadyCreating) => json_response(
+                StatusCode::TOO_MANY_REQUESTS,
+                HttpErrorBody::from_msg(e.to_string()),
+            ),
             Err(tenant::CreateTimelineError::AncestorLsn(err)) => json_response(
                 StatusCode::NOT_ACCEPTABLE,
                 HttpErrorBody::from_msg(format!("{err:#}")),
diff --git a/test_runner/regress/test_tenants.py b/test_runner/regress/test_tenants.py
index f8701b65d7d9..2832304dcce9 100644
--- a/test_runner/regress/test_tenants.py
+++ b/test_runner/regress/test_tenants.py
@@ -389,6 +389,9 @@ def create_bg(delay_ms):
             if e.status_code == 409:
                 log.info(f"delay_ms={delay_ms} 409")
                 pass
+            elif e.status_code == 429:
+                log.info(f"delay_ms={delay_ms} 429")
+                pass
             elif e.status_code == 400:
                 if "is less than existing" in e.message:
                     # We send creation requests very close together in time: it is expected that these