diff --git a/Lib/_pyrepl/completing_reader.py b/Lib/_pyrepl/completing_reader.py
index 9d2d43be5144e8..8d7ddd64f1e66a 100644
--- a/Lib/_pyrepl/completing_reader.py
+++ b/Lib/_pyrepl/completing_reader.py
@@ -41,11 +41,11 @@ def prefix(wordlist: list[str], j: int = 0) -> str:
             for word in wordlist:
                 d[word[i]] = 1
             if len(d) > 1:
-                return wordlist[0][j:i]
+                return wordlist[0][:i]
             i += 1
             d = {}
     except IndexError:
-        return wordlist[0][j:i]
+        return wordlist[0][:i]
     return ""
 
 
@@ -181,10 +181,16 @@ def do(self) -> None:
             if completions_unchangable and len(completions[0]) == len(stem):
                 r.msg = "[ sole completion ]"
                 r.dirty = True
-            r.insert(completions[0][len(stem):])
+            stem_len = len(stem)
+            del r.buffer[r.pos - stem_len:r.pos]
+            r.pos -= stem_len
+            r.insert(completions[0])
         else:
             p = prefix(completions, len(stem))
             if p:
+                stem_len = len(stem)
+                del r.buffer[r.pos - stem_len:r.pos]
+                r.pos -= stem_len
                 r.insert(p)
             if last_is_completer:
                 r.cmpltn_menu_visible = True
diff --git a/Lib/test/test_pyrepl/test_pyrepl.py b/Lib/test/test_pyrepl/test_pyrepl.py
index 35a1733787e7a2..428ab879ceafb1 100644
--- a/Lib/test/test_pyrepl/test_pyrepl.py
+++ b/Lib/test/test_pyrepl/test_pyrepl.py
@@ -936,6 +936,25 @@ def test_func(self):
         self.assertEqual(output, "dummy.test_func.__")
         self.assertEqual(mock_stderr.getvalue(), "")
 
+    def test_completion_replaces_input(self):
+        matches = []
+        def case_insensitive_completer(text, state):
+            nonlocal matches
+            candidates = ["PYTHON", "PYREPL"]
+            if state == 0:
+                matches = [c for c in candidates if c.lower().startswith(text.lower())]
+            if state < len(matches):
+                return matches[state]
+            return None
+
+        events = code_to_events("s='pyt\t'\ns='py\t\tr\t'\n")
+        reader = self.prepare_reader(events, {})
+        reader.config.readline_completer = case_insensitive_completer
+        output = multiline_input(reader)
+        self.assertEqual(output, "s='PYTHON'")
+
+        output = multiline_input(reader)
+        self.assertEqual(output, "s='PYREPL'")
 
 class TestPyReplModuleCompleter(TestCase):
     def setUp(self):
diff --git a/Misc/NEWS.d/next/Library/2026-03-01-23-27-19.gh-issue-145392.uiNk5Y.rst b/Misc/NEWS.d/next/Library/2026-03-01-23-27-19.gh-issue-145392.uiNk5Y.rst
new file mode 100644
index 00000000000000..4b533e277fffe2
--- /dev/null
+++ b/Misc/NEWS.d/next/Library/2026-03-01-23-27-19.gh-issue-145392.uiNk5Y.rst
@@ -0,0 +1 @@
+Fix :mod:`!_pyrepl` completion to replace input stem instead of appending.