diff --git a/changelog/10169.bugfix.rst b/changelog/10169.bugfix.rst
new file mode 100644
index 000000000..cbf3516a9
--- /dev/null
+++ b/changelog/10169.bugfix.rst
@@ -0,0 +1 @@
+Fix bug where very long option names could cause pytest to break with ``OSError: [Errno 36] File name too long`` on some systems.
diff --git a/src/_pytest/config/__init__.py b/src/_pytest/config/__init__.py
index 25cf75e98..74905ff4c 100644
--- a/src/_pytest/config/__init__.py
+++ b/src/_pytest/config/__init__.py
@@ -556,19 +556,13 @@ class PytestPluginManager(PluginManager):
                 path = path[:i]
             anchor = absolutepath(current / path)
 
-            # On Python 3.7 on Windows, anchor.exists() might raise
-            # if the anchor contains glob characters (for example "*//tests"), specially
-            # in the case of the 'testpaths' ini option.
-            # Using an explicit version check to remove this code later once
-            # Python 3.7 is dropped.
-            if sys.version_info[:2] == (3, 7):
-                try:
-                    anchor_exists = anchor.exists()
-                except OSError:  # pragma: no cover
-                    anchor_exists = False
-            else:
+            # Ensure we do not break if what appears to be an anchor
+            # is in fact a very long option (#10169).
+            try:
                 anchor_exists = anchor.exists()
-            if anchor_exists:  # We found some file object.
+            except OSError:  # pragma: no cover
+                anchor_exists = False
+            if anchor_exists:
                 self._try_load_conftest(anchor, namespace.importmode, rootpath)
                 foundanchor = True
         if not foundanchor:
diff --git a/testing/test_collection.py b/testing/test_collection.py
index f78ae7bea..bbcb358b6 100644
--- a/testing/test_collection.py
+++ b/testing/test_collection.py
@@ -1254,7 +1254,7 @@ def test_initial_conftests_with_testpaths(pytester: Pytester) -> None:
         textwrap.dedent(
             """
             def pytest_sessionstart(session):
-                raise Exception("pytest_sessionstart hook is successfully run")
+                raise Exception("pytest_sessionstart hook successfully run")
             """
         )
     )
@@ -1266,10 +1266,29 @@ def test_initial_conftests_with_testpaths(pytester: Pytester) -> None:
     )
     result = pytester.runpytest()
     result.stdout.fnmatch_lines(
-        "INTERNALERROR* Exception: pytest_sessionstart hook is successfully run"
+        "INTERNALERROR* Exception: pytest_sessionstart hook successfully run"
     )
 
 
+def test_large_option_breaks_initial_conftests(pytester: Pytester) -> None:
+    """Long option values do not break initial conftests handling (#10169)."""
+    option_value = "x" * 1024 * 1000
+    pytester.makeconftest(
+        """
+        def pytest_addoption(parser):
+            parser.addoption("--xx", default=None)
+        """
+    )
+    pytester.makepyfile(
+        f"""
+        def test_foo(request):
+            assert request.config.getoption("xx") == {option_value!r}
+        """
+    )
+    result = pytester.runpytest(f"--xx={option_value}")
+    assert result.ret == 0
+
+
 def test_collect_symlink_file_arg(pytester: Pytester) -> None:
     """Collect a direct symlink works even if it does not match python_files (#4325)."""
     real = pytester.makepyfile(