diff --git a/lib/galaxy/job_execution/setup.py b/lib/galaxy/job_execution/setup.py
index addb3bb4b3f..b7c1de94110 100644
--- a/lib/galaxy/job_execution/setup.py
+++ b/lib/galaxy/job_execution/setup.py
@@ -393,20 +393,13 @@ class JobWorkingDirectory:
     def create(self) -> str:
         """Create the working directory and return its path.
 
-        Raises ``FileExistsError`` if the per-job directory already exists
-        (job id collision or leftover from a crashed run).
+        Idempotent: if the per-job directory already exists (e.g. wrapper
+        reconstruction for a resubmitted job), it is returned without error.
         """
         if custom_path := self._custom_path:
             validate_working_directory_path(custom_path)
             path = self._per_job_path(custom_path)
-            try:
-                os.makedirs(path, exist_ok=False)
-            except FileExistsError as exc:
-                raise FileExistsError(
-                    f"Job working directory already exists for job {self._job.id} "
-                    f"at {path!r}; this indicates a job id collision or a leftover "
-                    f"directory from a previous run."
-                ) from exc
+            os.makedirs(path, exist_ok=True)
             return path
         self._object_store.create(
             self._job,
diff --git a/test/unit/job_execution/test_job_working_directory.py b/test/unit/job_execution/test_job_working_directory.py
index 28d1f21b3bc..b1f24818441 100644
--- a/test/unit/job_execution/test_job_working_directory.py
+++ b/test/unit/job_execution/test_job_working_directory.py
@@ -68,15 +68,17 @@ class TestJobWorkingDirectoryCustomPath:
         # The base must exist too (as parent of the per-job dir).
         assert os.path.isdir(base)
 
-    def test_create_raises_on_preexisting_per_job_dir(self, tmp_path, object_store):
+    def test_create_is_idempotent_on_preexisting_per_job_dir(self, tmp_path, object_store):
+        """create() returns the same path without error if the directory already exists."""
         base = str(tmp_path / "jobs")
         job = _make_job(100)
         job.working_directory = base
         jwd = JobWorkingDirectory(job, object_store)
 
-        jwd.create()
-        with pytest.raises(FileExistsError, match="already exists for job 100"):
-            jwd.create()
+        path1 = jwd.create()
+        path2 = jwd.create()
+        assert path1 == path2
+        assert os.path.isdir(path1)
 
     def test_exists_reflects_per_job_dir(self, tmp_path, object_store):
         base = str(tmp_path / "jobs")