diff --git a/Lib/test/test_os.py b/Lib/test/test_os.py
index 2a4ae1573ef599..42a08d83bb74e0 100644
--- a/Lib/test/test_os.py
+++ b/Lib/test/test_os.py
@@ -3513,6 +3513,33 @@ def test_set_inheritable_cloexec(self):
         self.assertEqual(fcntl.fcntl(fd, fcntl.F_GETFD) & fcntl.FD_CLOEXEC,
                          0)
 
+    @unittest.skipUnless(hasattr(os, 'O_PATH'), "need os.O_PATH")
+    def test_get_set_inheritable_o_path(self):
+        fd = os.open(__file__, os.O_PATH)
+        self.addCleanup(os.close, fd)
+        self.assertEqual(os.get_inheritable(fd), False)
+
+        os.set_inheritable(fd, True)
+        self.assertEqual(os.get_inheritable(fd), True)
+
+        os.set_inheritable(fd, False)
+        self.assertEqual(os.get_inheritable(fd), False)
+
+    def test_get_set_inheritable_badf(self):
+        fd = os_helper.make_bad_fd()
+
+        with self.assertRaises(OSError) as ctx:
+            os.get_inheritable(fd)
+        self.assertEqual(ctx.exception.errno, errno.EBADF)
+
+        with self.assertRaises(OSError) as ctx:
+            os.set_inheritable(fd, True)
+        self.assertEqual(ctx.exception.errno, errno.EBADF)
+
+        with self.assertRaises(OSError) as ctx:
+            os.set_inheritable(fd, False)
+        self.assertEqual(ctx.exception.errno, errno.EBADF)
+
     def test_open(self):
         fd = os.open(__file__, os.O_RDONLY)
         self.addCleanup(os.close, fd)
diff --git a/Misc/NEWS.d/next/Library/2021-01-08-15-49-20.bpo-42780.rtqi6B.rst b/Misc/NEWS.d/next/Library/2021-01-08-15-49-20.bpo-42780.rtqi6B.rst
new file mode 100644
index 00000000000000..a491690507129e
--- /dev/null
+++ b/Misc/NEWS.d/next/Library/2021-01-08-15-49-20.bpo-42780.rtqi6B.rst
@@ -0,0 +1 @@
+Fix os.set_inheritable() for O_PATH file descriptors on Linux.
diff --git a/Python/fileutils.c b/Python/fileutils.c
index 25516c23bf7ab4..fd2d5faa0fdf7e 100644
--- a/Python/fileutils.c
+++ b/Python/fileutils.c
@@ -1165,6 +1165,13 @@ set_inheritable(int fd, int inheritable, int raise, int *atomic_flag_works)
             return 0;
         }
 
+#ifdef __linux__
+        if (errno == EBADF) {
+            // On Linux, ioctl(FIOCLEX) will fail with EBADF for O_PATH file descriptors
+            // Fall through to the fcntl() path
+        }
+        else
+#endif
         if (errno != ENOTTY && errno != EACCES) {
             if (raise)
                 PyErr_SetFromErrno(PyExc_OSError);