diff --git a/CHANGES.rst b/CHANGES.rst
index fd46c84c..7da206f1 100644
--- a/CHANGES.rst
+++ b/CHANGES.rst
@@ -47,6 +47,9 @@ Unreleased
     loader thread. :issue:`4460`
 -   Deleting the session cookie uses the ``httponly`` flag.
     :issue:`4485`
+-   Relax typing for ``errorhandler`` to allow the user to use more
+    precise types and decorate the same function multiple times.
+    :issue:`4095, 4295, 4297`
 
 
 Version 2.0.3
diff --git a/src/flask/app.py b/src/flask/app.py
index aab5745d..854a796e 100644
--- a/src/flask/app.py
+++ b/src/flask/app.py
@@ -1265,9 +1265,7 @@ class Flask(Scaffold):
         self.shell_context_processors.append(f)
         return f
 
-    def _find_error_handler(
-        self, e: Exception
-    ) -> t.Optional["ErrorHandlerCallable[Exception]"]:
+    def _find_error_handler(self, e: Exception) -> t.Optional["ErrorHandlerCallable"]:
         """Return a registered error handler for an exception in this order:
         blueprint handler for a specific code, app handler for a specific code,
         blueprint handler for an exception class, app handler for an exception
diff --git a/src/flask/blueprints.py b/src/flask/blueprints.py
index 47465ad7..5d3b4e22 100644
--- a/src/flask/blueprints.py
+++ b/src/flask/blueprints.py
@@ -574,9 +574,7 @@ class Blueprint(Scaffold):
         handler is used for all requests, even if outside of the blueprint.
         """
 
-        def decorator(
-            f: "ErrorHandlerCallable[Exception]",
-        ) -> "ErrorHandlerCallable[Exception]":
+        def decorator(f: "ErrorHandlerCallable") -> "ErrorHandlerCallable":
             self.record_once(lambda s: s.app.errorhandler(code)(f))
             return f
 
diff --git a/src/flask/scaffold.py b/src/flask/scaffold.py
index 1d134435..acf8708b 100644
--- a/src/flask/scaffold.py
+++ b/src/flask/scaffold.py
@@ -21,7 +21,6 @@ from .templating import _default_template_ctx_processor
 from .typing import AfterRequestCallable
 from .typing import AppOrBlueprintKey
 from .typing import BeforeRequestCallable
-from .typing import GenericException
 from .typing import TeardownCallable
 from .typing import TemplateContextProcessorCallable
 from .typing import URLDefaultCallable
@@ -145,10 +144,7 @@ class Scaffold:
         #: directly and its format may change at any time.
         self.error_handler_spec: t.Dict[
             AppOrBlueprintKey,
-            t.Dict[
-                t.Optional[int],
-                t.Dict[t.Type[Exception], "ErrorHandlerCallable[Exception]"],
-            ],
+            t.Dict[t.Optional[int], t.Dict[t.Type[Exception], "ErrorHandlerCallable"]],
         ] = defaultdict(lambda: defaultdict(dict))
 
         #: A data structure of functions to call at the beginning of
@@ -652,11 +648,8 @@ class Scaffold:
 
     @setupmethod
     def errorhandler(
-        self, code_or_exception: t.Union[t.Type[GenericException], int]
-    ) -> t.Callable[
-        ["ErrorHandlerCallable[GenericException]"],
-        "ErrorHandlerCallable[GenericException]",
-    ]:
+        self, code_or_exception: t.Union[t.Type[Exception], int]
+    ) -> t.Callable[["ErrorHandlerCallable"], "ErrorHandlerCallable"]:
         """Register a function to handle errors by code or exception class.
 
         A decorator that is used to register a function given an
@@ -686,9 +679,7 @@ class Scaffold:
                                   an arbitrary exception
         """
 
-        def decorator(
-            f: "ErrorHandlerCallable[GenericException]",
-        ) -> "ErrorHandlerCallable[GenericException]":
+        def decorator(f: "ErrorHandlerCallable") -> "ErrorHandlerCallable":
             self.register_error_handler(code_or_exception, f)
             return f
 
@@ -697,8 +688,8 @@ class Scaffold:
     @setupmethod
     def register_error_handler(
         self,
-        code_or_exception: t.Union[t.Type[GenericException], int],
-        f: "ErrorHandlerCallable[GenericException]",
+        code_or_exception: t.Union[t.Type[Exception], int],
+        f: "ErrorHandlerCallable",
     ) -> None:
         """Alternative error attach function to the :meth:`errorhandler`
         decorator that is more straightforward to use for non decorator
@@ -722,9 +713,7 @@ class Scaffold:
                 " instead."
             ) from None
 
-        self.error_handler_spec[None][code][exc_class] = t.cast(
-            "ErrorHandlerCallable[Exception]", f
-        )
+        self.error_handler_spec[None][code][exc_class] = f
 
     @staticmethod
     def _get_exc_class_and_code(
diff --git a/src/flask/typing.py b/src/flask/typing.py
index 93896f80..bd8e61dc 100644
--- a/src/flask/typing.py
+++ b/src/flask/typing.py
@@ -33,8 +33,6 @@ ResponseReturnValue = t.Union[
     "WSGIApplication",
 ]
 
-GenericException = t.TypeVar("GenericException", bound=Exception, contravariant=True)
-
 AppOrBlueprintKey = t.Optional[str]  # The App key is None, whereas blueprints are named
 AfterRequestCallable = t.Callable[["Response"], "Response"]
 BeforeFirstRequestCallable = t.Callable[[], None]
@@ -46,4 +44,10 @@ TemplateGlobalCallable = t.Callable[..., t.Any]
 TemplateTestCallable = t.Callable[..., bool]
 URLDefaultCallable = t.Callable[[str, dict], None]
 URLValuePreprocessorCallable = t.Callable[[t.Optional[str], t.Optional[dict]], None]
-ErrorHandlerCallable = t.Callable[[GenericException], ResponseReturnValue]
+# This should take Exception, but that either breaks typing the argument
+# with a specific exception, or decorating multiple times with different
+# exceptions (and using a union type on the argument).
+# https://github.com/pallets/flask/issues/4095
+# https://github.com/pallets/flask/issues/4295
+# https://github.com/pallets/flask/issues/4297
+ErrorHandlerCallable = t.Callable[[t.Any], ResponseReturnValue]