diff --git a/docs/examples/demo_widgets/optional.py b/docs/examples/demo_widgets/optional.py
index 6fa88fd94..90d6cdcf5 100644
--- a/docs/examples/demo_widgets/optional.py
+++ b/docs/examples/demo_widgets/optional.py
@@ -3,14 +3,12 @@
 Optional user input using a dropdown selection widget.
 """
 
-from typing import Optional
-
 from magicgui import magicgui
 
 
 # Using optional will add a '----' to the combobox, which returns "None"
 @magicgui(path={"choices": ["a", "b"]})
-def f(path: Optional[str] = None):
+def f(path: str | None = None):
     """Öptional user input function."""
     print(path, type(path))
 
diff --git a/pyproject.toml b/pyproject.toml
index ec012096c..0efc26e4a 100644
--- a/pyproject.toml
+++ b/pyproject.toml
@@ -161,12 +161,10 @@ select = [
 ]
 ignore = [
     "D401", # First line should be in imperative mood
-    # magicgui resolves annotations at *runtime*, and on python < 3.14
-    # `get_origin(int | None)` is `types.UnionType`, not `typing.Union` -- so
-    # rewriting Optional/Union to PEP 604 changes behaviour rather than just
-    # spelling. Tests also deliberately exercise both spellings.
+    # `Union` is still needed as a runtime *value* for the public type aliases
+    # (PathLike, ChoicesType, AppRef, TableData, ...) and for `Union[args]`
+    # construction; ruff offers no fix for those, so the rule can't be enabled.
     "UP007", # Use `X | Y` for type annotations
-    "UP045", # Use `X | None` for type annotations
 ]
 
 [tool.ruff.lint.flake8-type-checking]
@@ -176,8 +174,10 @@ ignore = [
 exempt-modules = ["typing", "typing_extensions", "collections.abc"]
 
 [tool.ruff.lint.per-file-ignores]
-"tests/*.py" = ["D", "S", "E501"]
-"tests/test_util.py" = ["D", "S", "E501", "UP006"]
+# tests deliberately exercise both `Union[X, Y]` and `X | Y` spellings,
+# so they must not be rewritten to one of them (see test_no_order)
+"tests/*.py" = ["D", "S", "E501", "UP007", "UP045"]
+"tests/test_util.py" = ["D", "S", "E501", "UP006", "UP007", "UP045"]
 "docs/*.py" = ["B"]
 "docs/examples/*.py" = ["D", "B", "E501"]
 "src/magicgui/widgets/_image/*.py" = ["D"]
diff --git a/src/magicgui/_type_resolution.py b/src/magicgui/_type_resolution.py
index e3d0137b4..f402f2ca1 100644
--- a/src/magicgui/_type_resolution.py
+++ b/src/magicgui/_type_resolution.py
@@ -4,7 +4,7 @@
 from copy import copy
 from functools import lru_cache, partial
 from importlib import import_module
-from typing import Any, Optional, Union, get_type_hints
+from typing import Any, Union, get_type_hints
 
 try:
     from toolz import curry
@@ -27,8 +27,8 @@ def _unwrap_partial(func: Any) -> Any:
 
 def resolve_types(
     obj: Union[Callable, types.ModuleType, types.MethodType, type],
-    globalns: Optional[dict[str, Any]] = None,
-    localns: Optional[dict[str, Any]] = None,
+    globalns: dict[str, Any] | None = None,
+    localns: dict[str, Any] | None = None,
     do_imports: bool = False,
 ) -> dict[str, Any]:
     """Resolve type hints from an object.
@@ -80,8 +80,8 @@ def _resolve_forwards(v: Any) -> Any:
 
 def resolve_single_type(
     hint: Any,
-    globalns: Optional[dict[str, Any]] = None,
-    localns: Optional[dict[str, Any]] = None,
+    globalns: dict[str, Any] | None = None,
+    localns: dict[str, Any] | None = None,
     do_imports: bool = True,
 ) -> Any:
     """Resolve a single type hint.
diff --git a/src/magicgui/_util.py b/src/magicgui/_util.py
index 5c9fcfa72..3cc970f34 100644
--- a/src/magicgui/_util.py
+++ b/src/magicgui/_util.py
@@ -4,11 +4,14 @@
 import os
 import sys
 import time
+import types
 from collections.abc import Callable
 from functools import wraps
 from pathlib import Path
 from typing import (
     TYPE_CHECKING,
+    Any,
+    Union,
     get_args,
     get_origin,
     overload,
@@ -27,6 +30,16 @@
     C = TypeVar("C", bound=type)
 
 
+def is_union(annotation: Any) -> bool:
+    """Return True if `annotation` is a union, in either spelling.
+
+    `Union[X, Y]` and `X | Y` have different origins (`typing.Union` and
+    `types.UnionType`) on python < 3.14, so both must be checked.
+    """
+    origin = get_origin(annotation)
+    return origin is Union or origin is types.UnionType
+
+
 @overload
 def debounce(function: Callable[P, T]) -> Callable[P, T | None]: ...
 
diff --git a/src/magicgui/backends/_ipynb/application.py b/src/magicgui/backends/_ipynb/application.py
index b84504d9a..364b61bfc 100644
--- a/src/magicgui/backends/_ipynb/application.py
+++ b/src/magicgui/backends/_ipynb/application.py
@@ -1,7 +1,7 @@
 from __future__ import annotations
 
 import asyncio
-from typing import Callable
+from collections.abc import Callable
 
 from magicgui.widgets.protocols import BaseApplicationBackend
 
diff --git a/src/magicgui/schema/_ui_field.py b/src/magicgui/schema/_ui_field.py
index 0ab019212..c93b3c181 100644
--- a/src/magicgui/schema/_ui_field.py
+++ b/src/magicgui/schema/_ui_field.py
@@ -21,6 +21,7 @@
     get_origin,
 )
 
+from magicgui._util import is_union
 from magicgui.types import JsonStringFormats, Undefined, _Undefined
 
 if TYPE_CHECKING:
@@ -53,7 +54,7 @@ class UiField(Generic[T]):
 
     def __post_init__(self) -> None:
         """Coerce Optional[...] to nullable and remove it from the type."""
-        if get_origin(self.type) is Union:
+        if is_union(self.type):
             args = get_args(self.type)
             nonnull = tuple(a for a in args if a is not type(None))
             if len(nonnull) < len(args):
@@ -601,7 +602,7 @@ def _uifield_from_pydantic2(finfo: FieldInfo, name: str) -> UiField:
     )
 
     nullable = None
-    if get_origin(finfo.annotation) is Union and any(
+    if is_union(finfo.annotation) and any(
         i for i in get_args(finfo.annotation) if i is type(None)
     ):
         nullable = True
diff --git a/src/magicgui/type_map/_type_map.py b/src/magicgui/type_map/_type_map.py
index 62f2d35ff..48de51efa 100644
--- a/src/magicgui/type_map/_type_map.py
+++ b/src/magicgui/type_map/_type_map.py
@@ -32,7 +32,7 @@
 
 from magicgui import widgets
 from magicgui._type_resolution import resolve_single_type
-from magicgui._util import safe_issubclass
+from magicgui._util import is_union, safe_issubclass
 from magicgui.application import AppRef, use_app
 from magicgui.types import PathLike, ReturnCallback, Undefined, _Undefined
 from magicgui.widgets import protocols
@@ -994,7 +994,7 @@ def _register_type_callback(
         _validate_return_callback(return_callback)
         # if the type is a Union, add the callback to all of the types in the union
         # (except NoneType)
-        if get_origin(resolved_type) is Union:
+        if is_union(resolved_type):
             for type_per in _generate_union_variants(resolved_type):
                 if return_callback not in self._return_callbacks[type_per]:
                     self._return_callbacks[type_per].append(return_callback)
diff --git a/src/magicgui/widgets/_image/_mpl_image.py b/src/magicgui/widgets/_image/_mpl_image.py
index 514652718..189251079 100644
--- a/src/magicgui/widgets/_image/_mpl_image.py
+++ b/src/magicgui/widgets/_image/_mpl_image.py
@@ -54,7 +54,7 @@
 import logging
 from collections.abc import Collection
 from functools import lru_cache
-from typing import TYPE_CHECKING, Optional, Union
+from typing import TYPE_CHECKING, Union
 
 try:
     import numpy as np
@@ -513,7 +513,7 @@ def __init__(self, cmap=None, norm=None):
     def set_data(
         self,
         A: Union[str, "Path", "np.ndarray", "PIL.Image.Image"],
-        format: Optional[str] = None,
+        format: str | None = None,
     ):
         """Set the image array.
 
diff --git a/src/magicgui/widgets/bases/_value_widget.py b/src/magicgui/widgets/bases/_value_widget.py
index 96c0fc271..fbc13eefd 100644
--- a/src/magicgui/widgets/bases/_value_widget.py
+++ b/src/magicgui/widgets/bases/_value_widget.py
@@ -7,14 +7,13 @@
     Any,
     Generic,
     TypeVar,
-    Union,
     cast,
     get_args,
-    get_origin,
 )
 
 from psygnal import Signal
 
+from magicgui._util import is_union
 from magicgui.types import Undefined, _Undefined
 
 from ._widget import Widget
@@ -167,7 +166,7 @@ def annotation(self) -> Any:
         annotation will return the first argument in the Optional clause.
         """
         annotation = Widget.annotation.fget(self)  # type: ignore
-        if self._nullable and get_origin(annotation) is Union:
+        if self._nullable and is_union(annotation):
             return get_args(annotation)[0]
         return annotation
 
diff --git a/tests/test_types.py b/tests/test_types.py
index 14ff41cc0..f7008ce9a 100644
--- a/tests/test_types.py
+++ b/tests/test_types.py
@@ -247,3 +247,36 @@ def f(a: int, b: str):
     assert isinstance(fgui0[1], widgets.LineEdit)
     assert isinstance(fgui1[0], widgets.Slider)
     assert isinstance(fgui1[1], widgets.LineEdit)
+
+
+def test_pep604_union_matches_typing_union():
+    """`X | None` should behave exactly like `Optional[X]`.
+
+    On python < 3.14 `get_origin(int | None)` is `types.UnionType` rather than
+    `typing.Union`, so anything comparing against `Union` must accept both.
+    """
+    old = widgets.create_widget(annotation=Optional[int])
+    new = widgets.create_widget(annotation=int | None)
+
+    assert type(new) is type(old)
+    assert new._nullable is old._nullable is True
+    # the Optional wrapper is stripped from the reported annotation
+    assert new.annotation is old.annotation is int
+
+
+def test_pep604_union_return_callback():
+    """Registering `X | Y` should register each member, as `Union[X, Y]` does."""
+    mock = Mock()
+    register_type(int | str, return_callback=mock)
+    try:
+        # registering a union registers a callback for each member type
+        @magicgui
+        def f() -> int:
+            return 1
+
+        f()
+        mock.assert_called_once()
+    finally:
+        callbacks = TypeMap.global_instance()._return_callbacks
+        for key in (int, str, Union[int, str]):
+            callbacks.pop(key, None)