diff --git a/Lib/dbm/sqlite3.py b/Lib/dbm/sqlite3.py
index b296a1bcd1bbfa..42c04878d2f85c 100644
--- a/Lib/dbm/sqlite3.py
+++ b/Lib/dbm/sqlite3.py
@@ -60,6 +60,9 @@ def __init__(self, path, /, *, flag, mode):
         # We use the URI format when opening the database.
         uri = _normalize_uri(path)
         uri = f"{uri}?mode={flag}"
+        if flag == "ro":
+            # Add immutable=1 to allow read-only SQLite access even if wal/shm missing
+            uri += "&immutable=1"
 
         try:
             self._cx = sqlite3.connect(uri, autocommit=True, uri=True)
@@ -67,11 +70,12 @@ def __init__(self, path, /, *, flag, mode):
             raise error(str(exc))
 
         # This is an optimization only; it's ok if it fails.
-        with suppress(sqlite3.OperationalError):
-            self._cx.execute("PRAGMA journal_mode = wal")
+        if flag != "ro":
+            with suppress(sqlite3.OperationalError):
+                self._cx.execute("PRAGMA journal_mode = OFF")
 
-        if flag == "rwc":
-            self._execute(BUILD_TABLE)
+            if flag == "rwc":
+                self._execute(BUILD_TABLE)
 
     def _execute(self, *args, **kwargs):
         if not self._cx:
diff --git a/Lib/test/test_dbm_sqlite3.py b/Lib/test/test_dbm_sqlite3.py
index 9216da8a63f957..321ad41c7f36bc 100644
--- a/Lib/test/test_dbm_sqlite3.py
+++ b/Lib/test/test_dbm_sqlite3.py
@@ -1,3 +1,5 @@
+import os
+import stat
 import sys
 import unittest
 from contextlib import closing
@@ -89,6 +91,88 @@ def test_readonly_keys(self):
     def test_readonly_iter(self):
         self.assertEqual([k for k in self.db], [b"key1", b"key2"])
 
+class Immutable(unittest.TestCase):
+    def setUp(self):
+        self.filename = os_helper.TESTFN
+
+        db = dbm_sqlite3.open(self.filename, "c")
+        db[b"key"] = b"value"
+        db.close()
+
+        self.db = dbm_sqlite3.open(self.filename, "r")
+
+    def tearDown(self):
+        self.db.close()
+        for suffix in "", "-wal", "-shm":
+            os_helper.unlink(self.filename + suffix)
+
+    def test_readonly_open_without_wal_shm(self):
+        wal_path = self.filename + "-wal"
+        shm_path = self.filename + "-shm"
+
+        self.assertFalse(os.path.exists(wal_path))
+        self.assertFalse(os.path.exists(shm_path))
+
+        self.assertEqual(self.db[b"key"], b"value")
+
+
+class ReadOnlyFilesystem(unittest.TestCase):
+
+    def setUp(self):
+        self.test_dir = os_helper.TESTFN
+        os.mkdir(self.test_dir)
+        self.db_path = os.path.join(self.test_dir, "test.db")
+
+        db = dbm_sqlite3.open(self.db_path, "c")
+        db[b"key"] = b"value"
+        db.close()
+
+    def tearDown(self):
+        os.chmod(self.db_path, stat.S_IWRITE)
+        os.chmod(self.test_dir, stat.S_IWRITE | stat.S_IEXEC | stat.S_IREAD)
+        os_helper.rmtree(self.test_dir)
+
+    def test_open_readonly_dir_success_ro(self):
+        files = os.listdir(self.test_dir)
+        self.assertEqual(sorted(files), ["test.db"])
+
+        os.chmod(self.test_dir, stat.S_IREAD | stat.S_IEXEC)
+        with dbm_sqlite3.open(self.db_path, "r") as db:
+            self.assertEqual(db[b"key"], b"value")
+
+    def test_open_readonly_file_success(self):
+        os.chmod(self.db_path, stat.S_IREAD)
+        with dbm_sqlite3.open(self.db_path, "r") as db:
+            self.assertEqual(db[b"key"], b"value")
+
+    def test_open_readonly_file_fail_rw(self):
+        os.chmod(self.db_path, stat.S_IREAD)
+        with dbm_sqlite3.open(self.db_path, "w") as db:
+            with self.assertRaises(OSError):
+                db[b"newkey"] = b"newvalue"
+    @unittest.skipUnless(sys.platform == "darwin", "SQLite fallback behavior differs on non-macOS")
+    def test_open_readonly_dir_fail_rw_missing_wal_shm(self):
+        for suffix in ("-wal", "-shm"):
+            os_helper.unlink(self.db_path + suffix)
+
+        os.chmod(self.test_dir, stat.S_IREAD | stat.S_IEXEC)
+
+        with self.assertRaises(OSError):
+            with dbm_sqlite3.open(self.db_path, "w") as db:
+                db[b"newkey"] = b"newvalue"
+
+    @unittest.skipUnless(sys.platform == "darwin", "SQLite fallback behavior differs on non-macOS")
+    def test_open_readonly_dir_fail_rw_with_writable_db(self):
+        os.chmod(self.db_path, stat.S_IREAD | stat.S_IWRITE)
+        for suffix in ("-wal", "-shm"):
+            os_helper.unlink(self.db_path + suffix)
+
+        os.chmod(self.test_dir, stat.S_IREAD | stat.S_IEXEC)
+
+        with self.assertRaises(OSError):
+            with dbm_sqlite3.open(self.db_path, "w") as db:
+                db[b"newkey"] = b"newvalue"
+
 
 class ReadWrite(_SQLiteDbmTests):
 
diff --git a/Misc/NEWS.d/next/Library/2025-06-16-15-00-13.gh-issue-135386.lNrxLc.rst b/Misc/NEWS.d/next/Library/2025-06-16-15-00-13.gh-issue-135386.lNrxLc.rst
new file mode 100644
index 00000000000000..d3f81cb9201aaf
--- /dev/null
+++ b/Misc/NEWS.d/next/Library/2025-06-16-15-00-13.gh-issue-135386.lNrxLc.rst
@@ -0,0 +1 @@
+Fix :exc:`sqlite3.OperationalError` error when using :func:`dbm.open` with a read-only file object.