diff --git a/changelog/14327.bugfix.rst b/changelog/14327.bugfix.rst
new file mode 100644
index 00000000000..e1ad3a03468
--- /dev/null
+++ b/changelog/14327.bugfix.rst
@@ -0,0 +1 @@
+Fixed ``RaisesGroup.matches()`` so group-level ``check=`` callbacks are no longer called again on the first nested exception while building suggestion text.
diff --git a/src/_pytest/raises.py b/src/_pytest/raises.py
index 75eea7d8cc9..cbd0786a5c7 100644
--- a/src/_pytest/raises.py
+++ b/src/_pytest/raises.py
@@ -1210,12 +1210,12 @@ def matches(
             if (
                 len(actual_exceptions) == len(self.expected_exceptions) == 1
                 and isinstance(expected := self.expected_exceptions[0], type)
-                # we explicitly break typing here :)
-                and self._check_check(actual_exceptions[0])  # type: ignore[arg-type]
+                and isinstance(actual_exceptions[0], expected)
             ):
                 self._fail_reason = reason + (
-                    f", but did return True for the expected {self._repr_expected(expected)}."
-                    f" You might want RaisesGroup(RaisesExc({expected.__name__}, check=<...>))"
+                    f". If you meant to check the sub-exception instead of the group,"
+                    f" you might want "
+                    f"RaisesGroup(RaisesExc({expected.__name__}, check=<...>))"
                 )
             else:
                 self._fail_reason = reason
diff --git a/testing/python/raises_group.py b/testing/python/raises_group.py
index e5e3b5cd2dc..ff5b83009f0 100644
--- a/testing/python/raises_group.py
+++ b/testing/python/raises_group.py
@@ -417,7 +417,7 @@ def is_exc(e: ExceptionGroup[ValueError]) -> bool:
 
     with (
         fails_raises_group(
-            f"check {is_exc_repr} did not return True on the ExceptionGroup"
+            f"check {is_exc_repr} did not return True on the ExceptionGroup. If you meant to check the sub-exception instead of the group, you might want RaisesGroup(RaisesExc(ValueError, check=<...>))"
         ),
         RaisesGroup(ValueError, check=is_exc),
     ):
@@ -429,13 +429,49 @@ def is_value_error(e: BaseException) -> bool:
     # helpful suggestion if the user thinks the check is for the sub-exception
     with (
         fails_raises_group(
-            f"check {is_value_error} did not return True on the ExceptionGroup, but did return True for the expected ValueError. You might want RaisesGroup(RaisesExc(ValueError, check=<...>))"
+            f"check {is_value_error} did not return True on the ExceptionGroup. If you meant to check the sub-exception instead of the group, you might want RaisesGroup(RaisesExc(ValueError, check=<...>))"
         ),
         RaisesGroup(ValueError, check=is_value_error),
     ):
         raise ExceptionGroup("", (ValueError(),))
 
 
+def test_check_is_only_called_on_the_group() -> None:
+    calls: list[type[BaseException]] = []
+
+    def check(exc_group: ExceptionGroup[ValueError]) -> bool:
+        calls.append(type(exc_group))
+        return False
+
+    with (
+        fails_raises_group(
+            f"check {repr_callable(check)} did not return True on the ExceptionGroup. If you meant to check the sub-exception instead of the group, you might want RaisesGroup(RaisesExc(ValueError, check=<...>))"
+        ),
+        RaisesGroup(ValueError, check=check),
+    ):
+        raise ExceptionGroup("", (ValueError(),))
+
+    assert calls == [ExceptionGroup]
+
+
+def test_matches_check_is_only_called_on_the_group() -> None:
+    calls: list[type[BaseException]] = []
+
+    def check(exc_group: ExceptionGroup[ValueError]) -> bool:
+        calls.append(type(exc_group))
+        return False
+
+    matcher = RaisesGroup(ValueError, check=check)
+
+    assert not matcher.matches(ExceptionGroup("", (ValueError(),)))
+    assert matcher.fail_reason == (
+        f"check {repr_callable(check)} did not return True on the ExceptionGroup. "
+        "If you meant to check the sub-exception instead of the group, you might "
+        "want RaisesGroup(RaisesExc(ValueError, check=<...>))"
+    )
+    assert calls == [ExceptionGroup]
+
+
 def test_unwrapped_match_check() -> None:
     def my_check(e: object) -> bool:  # pragma: no cover
         return True