diff --git a/Lib/_pyio.py b/Lib/_pyio.py
index a870de5b532542..f79674fb7a9f5e 100644
--- a/Lib/_pyio.py
+++ b/Lib/_pyio.py
@@ -1563,7 +1563,8 @@ def __init__(self, file, mode='r', closefd=True, opener=None):
                     if not isinstance(fd, int):
                         raise TypeError('expected integer from opener')
                     if fd < 0:
-                        raise OSError('Negative file descriptor')
+                        # bpo-27066: Raise a ValueError for bad value.
+                        raise ValueError(f'opener returned {fd}')
                 owned_fd = fd
                 if not noinherit_flag:
                     os.set_inheritable(fd, False)
diff --git a/Lib/test/test_io.py b/Lib/test/test_io.py
index 5a8f1949baaa98..a12bd82fea9cd6 100644
--- a/Lib/test/test_io.py
+++ b/Lib/test/test_io.py
@@ -918,7 +918,7 @@ def test_bad_opener_negative_1(self):
         def badopener(fname, flags):
             return -1
         with self.assertRaises(ValueError) as cm:
-            open('non-existent', 'r', opener=badopener)
+            self.open('non-existent', 'r', opener=badopener)
         self.assertEqual(str(cm.exception), 'opener returned -1')
 
     def test_bad_opener_other_negative(self):
@@ -926,7 +926,7 @@ def test_bad_opener_other_negative(self):
         def badopener(fname, flags):
             return -2
         with self.assertRaises(ValueError) as cm:
-            open('non-existent', 'r', opener=badopener)
+            self.open('non-existent', 'r', opener=badopener)
         self.assertEqual(str(cm.exception), 'opener returned -2')
 
     def test_opener_invalid_fd(self):
diff --git a/Misc/NEWS.d/next/Library/2025-05-13-18-21-59.gh-issue-71253.-3Sf_K.rst b/Misc/NEWS.d/next/Library/2025-05-13-18-21-59.gh-issue-71253.-3Sf_K.rst
new file mode 100644
index 00000000000000..714d707f488709
--- /dev/null
+++ b/Misc/NEWS.d/next/Library/2025-05-13-18-21-59.gh-issue-71253.-3Sf_K.rst
@@ -0,0 +1,3 @@
+Raise :exc:`ValueError` in :func:`open` if *opener* returns a negative
+file-descriptor in the Python implementation of :mod:`io` to match the
+C implementation.