diff --git a/tests/unit/forklift/test_legacy.py b/tests/unit/forklift/test_legacy.py
index 2a81315a25eb..8fd337e68a4a 100644
--- a/tests/unit/forklift/test_legacy.py
+++ b/tests/unit/forklift/test_legacy.py
@@ -1,6 +1,7 @@
 # SPDX-License-Identifier: Apache-2.0
 
 import base64
+import builtins
 import hashlib
 import io
 import json
@@ -2031,6 +2032,95 @@ def test_upload_succeeds_custom_project_size_limit(
             ("example", "1.0", "add source file example-1.0.tar.gz", user),
         ]
 
+    def test_upload_fails_with_oserror_on_metadata_write(
+        self, tmpdir, monkeypatch, pyramid_config, db_request
+    ):
+        monkeypatch.setattr(tempfile, "tempdir", str(tmpdir))
+        monkeypatch.setattr(
+            legacy, "_is_valid_dist_file", lambda *a, **kw: (True, None)
+        )
+
+        user = UserFactory.create()
+        EmailFactory.create(user=user)
+        project = ProjectFactory.create()
+        release = ReleaseFactory.create(project=project, version="1.0")
+        RoleFactory.create(user=user, project=project)
+
+        filename = "{}-{}-py2.py3-none-any.whl".format(
+            project.normalized_name.replace("-", "_"),
+            release.version,
+        )
+
+        db_request.user = user
+        pyramid_config.testing_securitypolicy(identity=user)
+
+        db_request.user_agent = "warehouse-tests/6.6.6"
+
+        wheel_metadata = dedent(
+            """
+            Metadata-Version: 2.1
+            Name: {project.name}
+            Version: {release.version}
+            """
+        ).encode("utf-8")
+
+        wheel_testdata = _get_whl_testdata(
+            name=project.normalized_name.replace("-", "_"), version=release.version
+        )
+        wheel_md5 = hashlib.md5(wheel_testdata).hexdigest()
+
+        content = FieldStorage()
+        content.filename = filename
+        content.file = io.BytesIO(wheel_testdata)
+        content.type = "application/octet-stream"
+
+        db_request.POST = MultiDict(
+            {
+                "metadata_version": "2.1",
+                "name": project.name,
+                "version": release.version,
+                "filetype": "bdist_wheel",
+                "pyversion": "py2.py3",
+                "content": content,
+                "md5_digest": wheel_md5,
+                "wheel_metadata_version": "1.0",
+                "wheel_metadata": base64.b64encode(wheel_metadata).decode("ascii"),
+            }
+        )
+
+        storage_service = pretend.stub(store=lambda path, file_path, *, meta: None)
+        db_request.find_service = pretend.call_recorder(
+            lambda svc, name=None, context=None: {
+                IFileStorage: storage_service,
+            }.get(svc)
+        )
+
+        # Patch open to raise OSError
+        original_open = builtins.open
+
+        def mock_open(file, mode="r", *args, **kwargs):
+            if str(file).endswith(".metadata"):
+                raise OSError("Filename too long")
+            return original_open(file, mode, *args, **kwargs)
+
+        monkeypatch.setattr("builtins.open", mock_open)
+
+        with pytest.raises(HTTPBadRequest) as excinfo:
+            legacy.file_upload(db_request)
+
+        resp = excinfo.value
+
+        assert resp.status_code == 400
+        assert resp.status == f"400 Filename is too long: '{filename}'"
+
+        assert db_request.metrics.increment.calls == [
+            pretend.call("warehouse.upload.attempt"),
+            pretend.call(
+                "warehouse.upload.failed",
+                tags=["reason:filename-too-long", "filetype:bdist_wheel"],
+            ),
+        ]
+
     def test_upload_fails_with_previously_used_filename(
         self, pyramid_config, db_request
     ):
diff --git a/warehouse/forklift/legacy.py b/warehouse/forklift/legacy.py
index 5422785f6322..4e2745c7a026 100644
--- a/warehouse/forklift/legacy.py
+++ b/warehouse/forklift/legacy.py
@@ -1536,8 +1536,22 @@ def file_upload(request):
                         filename=filename, metadata_filename=metadata_filename
                     ),
                 )
-            with open(temporary_filename + ".metadata", "wb") as fp:
-                fp.write(wheel_metadata_contents)
+            try:
+                with open(temporary_filename + ".metadata", "wb") as fp:
+                    fp.write(wheel_metadata_contents)
+            except OSError:
+                request.metrics.increment(
+                    "warehouse.upload.failed",
+                    tags=[
+                        "reason:filename-too-long",
+                        f"filetype:{form.filetype.data}",
+                    ],
+                )
+                raise _exc_with_message(
+                    HTTPBadRequest,
+                    f"Filename is too long: '{filename}'",
+                )
+
             metadata_file_hashes = {
                 "sha256": hashlib.sha256(),
                 "blake2_256": hashlib.blake2b(digest_size=256 // 8),