diff --git a/Lib/test/test_zlib.py b/Lib/test/test_zlib.py
index 3243448043b5c2..a2468ab0ae6a38 100644
--- a/Lib/test/test_zlib.py
+++ b/Lib/test/test_zlib.py
@@ -1153,6 +1153,45 @@ def testDecompress(self):
         text = zlibd.decompress(self.DATA)
         self.assertEqual(text, self.TEXT)
 
+    def testDecompressZdictWrapped(self):
+        # gh-160001: for a zlib-wrapped stream zlib only announces the
+        # dictionary (``Z_NEED_DICT``) after the header, so it has to be
+        # applied from the decompression loop rather than the constructor.
+        zdict = b"hello world " * 10
+        compressor = zlib.compressobj(zdict=zdict)
+        data = compressor.compress(b"hello world hello") + compressor.flush()
+
+        decompressor = zlib._ZlibDecompressor(zdict=zdict)
+        self.assertEqual(decompressor.decompress(data), b"hello world hello")
+
+    def testDecompressZdictWrappedChunks(self):
+        zdict = b"hello world " * 10
+        compressor = zlib.compressobj(zdict=zdict)
+        data = compressor.compress(b"hello world hello") + compressor.flush()
+
+        decompressor = zlib._ZlibDecompressor(zdict=zdict)
+        result = b""
+        for index in range(0, len(data), 3):
+            result += decompressor.decompress(data[index:index + 3])
+
+        self.assertEqual(result, b"hello world hello")
+
+    def testDecompressZdictRaw(self):
+        zdict = b"hello world " * 10
+        compressor = zlib.compressobj(wbits=-zlib.MAX_WBITS, zdict=zdict)
+        data = compressor.compress(b"hello world hello") + compressor.flush()
+
+        decompressor = zlib._ZlibDecompressor(-zlib.MAX_WBITS, zdict=zdict)
+        self.assertEqual(decompressor.decompress(data), b"hello world hello")
+
+    def testDecompressFdictHeaderWithoutZdict(self):
+        # A zlib header with the FDICT flag set asks for a dictionary that was
+        # never provided; that is a zlib error, not an internal error.
+        fdict_header = b"\x78\xbb" + b"\x00\x00\x00\x01\x03\x00"
+
+        with self.assertRaises(zlib.error):
+            zlib._ZlibDecompressor().decompress(fdict_header)
+
     def testDecompressChunks10(self):
         zlibd = zlib._ZlibDecompressor()
         text = b''
diff --git a/Misc/NEWS.d/next/Library/2026-11-05-07-30-00.gh-issue-160001.Zq4WnH.rst b/Misc/NEWS.d/next/Library/2026-11-05-07-30-00.gh-issue-160001.Zq4WnH.rst
new file mode 100644
index 00000000000000..0e09743f828c9d
--- /dev/null
+++ b/Misc/NEWS.d/next/Library/2026-11-05-07-30-00.gh-issue-160001.Zq4WnH.rst
@@ -0,0 +1,4 @@
+:mod:`zlib`: Fix ``zlib._ZlibDecompressor`` failing with :exc:`SystemError`
+instead of decompressing when a ``zdict`` is passed for a zlib-wrapped stream.
+A stream that requires a dictionary which was not provided now raises
+:exc:`zlib.error`, matching ``zlib.Decompress``.
diff --git a/Modules/zlibmodule.c b/Modules/zlibmodule.c
index 31533fa047af0b..8b5d188a801b8d 100644
--- a/Modules/zlibmodule.c
+++ b/Modules/zlibmodule.c
@@ -1534,13 +1534,21 @@ decompress_buf(ZlibDecompressor *self, Py_ssize_t max_length)
                 break;
             default:
                 if (err == Z_NEED_DICT) {
-                    goto error;
+                    if (self->zdict == NULL) {
+                        zlib_error(state, self->zst, err,
+                                   "while decompressing data");
+                        goto error;
+                    }
+                    if (set_inflate_zdict_ZlibDecompressor(state, self) < 0) {
+                        goto error;
+                    }
+                    break;
                 }
                 else {
                     break;
                 }
             }
-        } while (self->zst.avail_out == 0);
+        } while (self->zst.avail_out == 0 || err == Z_NEED_DICT);
     } while(err != Z_STREAM_END && self->avail_in_real != 0);
 
     if (err == Z_STREAM_END) {