diff --git a/sanic/app.py b/sanic/app.py
index ca8c4fe0..01aa07cb 100644
--- a/sanic/app.py
+++ b/sanic/app.py
@@ -179,7 +179,9 @@ class Sanic(BaseSanic, metaclass=TouchUpMeta):
         self.configure_logging = configure_logging
         self.ctx = ctx or SimpleNamespace()
         self.debug = None
-        self.error_handler = error_handler or ErrorHandler()
+        self.error_handler = error_handler or ErrorHandler(
+            fallback=self.config.FALLBACK_ERROR_FORMAT,
+        )
         self.is_running = False
         self.is_stopping = False
         self.listeners: Dict[str, List[ListenerType]] = defaultdict(list)
diff --git a/sanic/blueprints.py b/sanic/blueprints.py
index fd7332aa..617ec606 100644
--- a/sanic/blueprints.py
+++ b/sanic/blueprints.py
@@ -266,6 +266,9 @@ class Blueprint(BaseSanic):
         opt_version = options.get("version", None)
         opt_strict_slashes = options.get("strict_slashes", None)
         opt_version_prefix = options.get("version_prefix", self.version_prefix)
+        error_format = options.get(
+            "error_format", app.config.FALLBACK_ERROR_FORMAT
+        )
 
         routes = []
         middleware = []
@@ -313,6 +316,7 @@ class Blueprint(BaseSanic):
                 future.unquote,
                 future.static,
                 version_prefix,
+                error_format,
             )
 
             route = app._apply_route(apply_route)
diff --git a/sanic/config.py b/sanic/config.py
index 2a90c5fb..2971f4e4 100644
--- a/sanic/config.py
+++ b/sanic/config.py
@@ -4,6 +4,7 @@ from pathlib import Path
 from typing import Any, Dict, Optional, Union
 from warnings import warn
 
+from sanic.errorpages import check_error_format
 from sanic.http import Http
 
 from .utils import load_module_from_file_location, str_to_bool
@@ -20,7 +21,7 @@ BASE_LOGO = """
 DEFAULT_CONFIG = {
     "ACCESS_LOG": True,
     "EVENT_AUTOREGISTER": False,
-    "FALLBACK_ERROR_FORMAT": "html",
+    "FALLBACK_ERROR_FORMAT": "auto",
     "FORWARDED_FOR_HEADER": "X-Forwarded-For",
     "FORWARDED_SECRET": None,
     "GRACEFUL_SHUTDOWN_TIMEOUT": 15.0,  # 15 sec
@@ -94,6 +95,7 @@ class Config(dict):
             self.load_environment_vars(SANIC_PREFIX)
 
         self._configure_header_size()
+        self._check_error_format()
 
     def __getattr__(self, attr):
         try:
@@ -109,6 +111,8 @@ class Config(dict):
             "REQUEST_MAX_SIZE",
         ):
             self._configure_header_size()
+        elif attr == "FALLBACK_ERROR_FORMAT":
+            self._check_error_format()
 
     def _configure_header_size(self):
         Http.set_header_max_size(
@@ -117,6 +121,9 @@ class Config(dict):
             self.REQUEST_MAX_SIZE,
         )
 
+    def _check_error_format(self):
+        check_error_format(self.FALLBACK_ERROR_FORMAT)
+
     def load_environment_vars(self, prefix=SANIC_PREFIX):
         """
         Looks for prefixed environment variables and applies
diff --git a/sanic/errorpages.py b/sanic/errorpages.py
index 5fc10de1..82cdd57a 100644
--- a/sanic/errorpages.py
+++ b/sanic/errorpages.py
@@ -340,41 +340,138 @@ RENDERERS_BY_CONFIG = {
 }
 
 RENDERERS_BY_CONTENT_TYPE = {
-    "multipart/form-data": HTMLRenderer,
-    "application/json": JSONRenderer,
     "text/plain": TextRenderer,
+    "application/json": JSONRenderer,
+    "multipart/form-data": HTMLRenderer,
+    "text/html": HTMLRenderer,
 }
+CONTENT_TYPE_BY_RENDERERS = {
+    v: k for k, v in RENDERERS_BY_CONTENT_TYPE.items()
+}
+
+RESPONSE_MAPPING = {
+    "empty": "html",
+    "json": "json",
+    "text": "text",
+    "raw": "text",
+    "html": "html",
+    "file": "html",
+    "file_stream": "text",
+    "stream": "text",
+    "redirect": "html",
+    "text/plain": "text",
+    "text/html": "html",
+    "application/json": "json",
+}
+
+
+def check_error_format(format):
+    if format not in RENDERERS_BY_CONFIG and format != "auto":
+        raise SanicException(f"Unknown format: {format}")
 
 
 def exception_response(
     request: Request,
     exception: Exception,
     debug: bool,
+    fallback: str,
+    base: t.Type[BaseRenderer],
     renderer: t.Type[t.Optional[BaseRenderer]] = None,
 ) -> HTTPResponse:
     """
     Render a response for the default FALLBACK exception handler.
     """
+    content_type = None
 
     if not renderer:
-        renderer = HTMLRenderer
+        # Make sure we have something set
+        renderer = base
+        render_format = fallback
 
         if request:
-            if request.app.config.FALLBACK_ERROR_FORMAT == "auto":
+            # If there is a request, try and get the format
+            # from the route
+            if request.route:
                 try:
-                    renderer = JSONRenderer if request.json else HTMLRenderer
-                except InvalidUsage:
+                    render_format = request.route.ctx.error_format
+                except AttributeError:
+                    ...
+
+            content_type = request.headers.getone("content-type", "").split(
+                ";"
+            )[0]
+
+            acceptable = request.accept
+
+            # If the format is auto still, make a guess
+            if render_format == "auto":
+                # First, if there is an Accept header, check if text/html
+                # is the first option
+                # According to MDN Web Docs, all major browsers use text/html
+                # as the primary value in Accept (with the exception of IE 8,
+                # and, well, if you are supporting IE 8, then you have bigger
+                # problems to concern yourself with than what default exception
+                # renderer is used)
+                # Source:
+                # https://developer.mozilla.org/en-US/docs/Web/HTTP/Content_negotiation/List_of_default_Accept_values
+
+                if acceptable and acceptable[0].match(
+                    "text/html",
+                    allow_type_wildcard=False,
+                    allow_subtype_wildcard=False,
+                ):
                     renderer = HTMLRenderer
 
-                content_type, *_ = request.headers.getone(
-                    "content-type", ""
-                ).split(";")
-                renderer = RENDERERS_BY_CONTENT_TYPE.get(
-                    content_type, renderer
-                )
+                # Second, if there is an Accept header, check if
+                # application/json is an option, or if the content-type
+                # is application/json
+                elif (
+                    acceptable
+                    and acceptable.match(
+                        "application/json",
+                        allow_type_wildcard=False,
+                        allow_subtype_wildcard=False,
+                    )
+                    or content_type == "application/json"
+                ):
+                    renderer = JSONRenderer
+
+                # Third, if there is no Accept header, assume we want text.
+                # The likely use case here is a raw socket.
+                elif not acceptable:
+                    renderer = TextRenderer
+                else:
+                    # Fourth, look to see if there was a JSON body
+                    # When in this situation, the request is probably coming
+                    # from curl, an API client like Postman or Insomnia, or a
+                    # package like requests or httpx
+                    try:
+                        # Give them the benefit of the doubt if they did:
+                        # $ curl localhost:8000 -d '{"foo": "bar"}'
+                        # And provide them with JSONRenderer
+                        renderer = JSONRenderer if request.json else base
+                    except InvalidUsage:
+                        renderer = base
             else:
-                render_format = request.app.config.FALLBACK_ERROR_FORMAT
                 renderer = RENDERERS_BY_CONFIG.get(render_format, renderer)
 
+            # Lastly, if there is an Accept header, make sure
+            # our choice is okay
+            if acceptable:
+                type_ = CONTENT_TYPE_BY_RENDERERS.get(renderer)  # type: ignore
+                if type_ and type_ not in acceptable:
+                    # If the renderer selected is not in the Accept header
+                    # look through what is in the Accept header, and select
+                    # the first option that matches. Otherwise, just drop back
+                    # to the original default
+                    for accept in acceptable:
+                        mtype = f"{accept.type_}/{accept.subtype}"
+                        maybe = RENDERERS_BY_CONTENT_TYPE.get(mtype)
+                        if maybe:
+                            renderer = maybe
+                            break
+                    else:
+                        renderer = base
+
     renderer = t.cast(t.Type[BaseRenderer], renderer)
     return renderer(request, exception, debug).render()
diff --git a/sanic/handlers.py b/sanic/handlers.py
index e33aff76..ffeb76b8 100644
--- a/sanic/handlers.py
+++ b/sanic/handlers.py
@@ -1,12 +1,13 @@
-from typing import List, Optional
+from typing import Dict, List, Optional, Tuple, Type
 
-from sanic.errorpages import exception_response
+from sanic.errorpages import BaseRenderer, HTMLRenderer, exception_response
 from sanic.exceptions import (
     ContentRangeError,
     HeaderNotFound,
     InvalidRangeType,
 )
 from sanic.log import error_logger
+from sanic.models.handler_types import RouteHandler
 from sanic.response import text
 
 
@@ -23,10 +24,15 @@ class ErrorHandler:
 
     """
 
-    def __init__(self):
-        self.handlers = []
-        self.cached_handlers = {}
+    # Beginning in v22.3, the base renderer will be TextRenderer
+    def __init__(self, fallback: str, base: Type[BaseRenderer] = HTMLRenderer):
+        self.handlers: List[Tuple[Type[BaseException], RouteHandler]] = []
+        self.cached_handlers: Dict[
+            Tuple[Type[BaseException], Optional[str]], Optional[RouteHandler]
+        ] = {}
         self.debug = False
+        self.fallback = fallback
+        self.base = base
 
     def add(self, exception, handler, route_names: Optional[List[str]] = None):
         """
@@ -142,7 +148,13 @@ class ErrorHandler:
         :return:
         """
         self.log(request, exception)
-        return exception_response(request, exception, self.debug)
+        return exception_response(
+            request,
+            exception,
+            debug=self.debug,
+            base=self.base,
+            fallback=self.fallback,
+        )
 
     @staticmethod
     def log(request, exception):
diff --git a/sanic/headers.py b/sanic/headers.py
index cc05f8e0..dbb8720f 100644
--- a/sanic/headers.py
+++ b/sanic/headers.py
@@ -35,7 +35,7 @@ _host_re = re.compile(
 
 def parse_arg_as_accept(f):
     def func(self, other, *args, **kwargs):
-        if not isinstance(other, Accept):
+        if not isinstance(other, Accept) and other:
             other = Accept.parse(other)
         return f(self, other, *args, **kwargs)
 
@@ -181,6 +181,27 @@ class Accept(str):
         return cls(mtype, MediaType(type_), MediaType(subtype), **params)
 
 
+class AcceptContainer(list):
+    def __contains__(self, o: object) -> bool:
+        return any(item.match(o) for item in self)
+
+    def match(
+        self,
+        o: object,
+        *,
+        allow_type_wildcard: bool = True,
+        allow_subtype_wildcard: bool = True,
+    ) -> bool:
+        return any(
+            item.match(
+                o,
+                allow_type_wildcard=allow_type_wildcard,
+                allow_subtype_wildcard=allow_subtype_wildcard,
+            )
+            for item in self
+        )
+
+
 def parse_content_header(value: str) -> Tuple[str, Options]:
     """Parse content-type and content-disposition header values.
 
@@ -356,7 +377,7 @@ def _sort_accept_value(accept: Accept):
     )
 
 
-def parse_accept(accept: str) -> List[Accept]:
+def parse_accept(accept: str) -> AcceptContainer:
     """Parse an Accept header and order the acceptable media types in
     accorsing to RFC 7231, s. 5.3.2
     https://datatracker.ietf.org/doc/html/rfc7231#section-5.3.2
@@ -370,4 +391,6 @@ def parse_accept(accept: str) -> List[Accept]:
 
         accept_list.append(Accept.parse(mtype))
 
-    return sorted(accept_list, key=_sort_accept_value, reverse=True)
+    return AcceptContainer(
+        sorted(accept_list, key=_sort_accept_value, reverse=True)
+    )
diff --git a/sanic/mixins/routes.py b/sanic/mixins/routes.py
index 6881f291..3d9733cd 100644
--- a/sanic/mixins/routes.py
+++ b/sanic/mixins/routes.py
@@ -1,17 +1,20 @@
+from ast import NodeVisitor, Return, parse
 from functools import partial, wraps
-from inspect import signature
+from inspect import getsource, signature
 from mimetypes import guess_type
 from os import path
 from pathlib import PurePath
 from re import sub
+from textwrap import dedent
 from time import gmtime, strftime
-from typing import Callable, Iterable, List, Optional, Set, Tuple, Union
+from typing import Any, Callable, Iterable, List, Optional, Set, Tuple, Union
 from urllib.parse import unquote
 
 from sanic_routing.route import Route  # type: ignore
 
 from sanic.compat import stat_async
 from sanic.constants import DEFAULT_HTTP_CONTENT_TYPE, HTTP_METHODS
+from sanic.errorpages import RESPONSE_MAPPING
 from sanic.exceptions import (
     ContentRangeError,
     FileNotFound,
@@ -61,6 +64,7 @@ class RouteMixin:
         unquote: bool = False,
         static: bool = False,
         version_prefix: str = "/v",
+        error_format: Optional[str] = None,
     ) -> RouteWrapper:
         """
         Decorate a function to be registered as a route
@@ -103,6 +107,7 @@ class RouteMixin:
             nonlocal websocket
             nonlocal static
             nonlocal version_prefix
+            nonlocal error_format
 
             if isinstance(handler, tuple):
                 # if a handler fn is already wrapped in a route, the handler
@@ -128,6 +133,9 @@ class RouteMixin:
                 # subprotocol is unordered, keep it unordered
                 subprotocols = frozenset(subprotocols)
 
+            if not error_format or error_format == "auto":
+                error_format = self._determine_error_format(handler)
+
             route = FutureRoute(
                 handler,
                 uri,
@@ -143,6 +151,7 @@ class RouteMixin:
                 unquote,
                 static,
                 version_prefix,
+                error_format,
             )
 
             self._future_routes.add(route)
@@ -186,6 +195,7 @@ class RouteMixin:
         name: Optional[str] = None,
         stream: bool = False,
         version_prefix: str = "/v",
+        error_format: Optional[str] = None,
     ) -> RouteHandler:
         """A helper method to register class instance or
         functions as a handler to the application url
@@ -236,6 +246,7 @@ class RouteMixin:
             version=version,
             name=name,
             version_prefix=version_prefix,
+            error_format=error_format,
         )(handler)
         return handler
 
@@ -249,6 +260,7 @@ class RouteMixin:
         name: Optional[str] = None,
         ignore_body: bool = True,
         version_prefix: str = "/v",
+        error_format: Optional[str] = None,
     ) -> RouteWrapper:
         """
         Add an API URL under the **GET** *HTTP* method
@@ -272,6 +284,7 @@ class RouteMixin:
             name=name,
             ignore_body=ignore_body,
             version_prefix=version_prefix,
+            error_format=error_format,
         )
 
     def post(
@@ -283,6 +296,7 @@ class RouteMixin:
         version: Optional[int] = None,
         name: Optional[str] = None,
         version_prefix: str = "/v",
+        error_format: Optional[str] = None,
     ) -> RouteWrapper:
         """
         Add an API URL under the **POST** *HTTP* method
@@ -306,6 +320,7 @@ class RouteMixin:
             version=version,
             name=name,
             version_prefix=version_prefix,
+            error_format=error_format,
         )
 
     def put(
@@ -317,6 +332,7 @@ class RouteMixin:
         version: Optional[int] = None,
         name: Optional[str] = None,
         version_prefix: str = "/v",
+        error_format: Optional[str] = None,
     ) -> RouteWrapper:
         """
         Add an API URL under the **PUT** *HTTP* method
@@ -340,6 +356,7 @@ class RouteMixin:
             version=version,
             name=name,
             version_prefix=version_prefix,
+            error_format=error_format,
         )
 
     def head(
@@ -351,6 +368,7 @@ class RouteMixin:
         name: Optional[str] = None,
         ignore_body: bool = True,
         version_prefix: str = "/v",
+        error_format: Optional[str] = None,
     ) -> RouteWrapper:
         """
         Add an API URL under the **HEAD** *HTTP* method
@@ -382,6 +400,7 @@ class RouteMixin:
             name=name,
             ignore_body=ignore_body,
             version_prefix=version_prefix,
+            error_format=error_format,
         )
 
     def options(
@@ -393,6 +412,7 @@ class RouteMixin:
         name: Optional[str] = None,
         ignore_body: bool = True,
         version_prefix: str = "/v",
+        error_format: Optional[str] = None,
     ) -> RouteWrapper:
         """
         Add an API URL under the **OPTIONS** *HTTP* method
@@ -424,6 +444,7 @@ class RouteMixin:
             name=name,
             ignore_body=ignore_body,
             version_prefix=version_prefix,
+            error_format=error_format,
         )
 
     def patch(
@@ -435,6 +456,7 @@ class RouteMixin:
         version: Optional[int] = None,
         name: Optional[str] = None,
         version_prefix: str = "/v",
+        error_format: Optional[str] = None,
     ) -> RouteWrapper:
         """
         Add an API URL under the **PATCH** *HTTP* method
@@ -468,6 +490,7 @@ class RouteMixin:
             version=version,
             name=name,
             version_prefix=version_prefix,
+            error_format=error_format,
         )
 
     def delete(
@@ -479,6 +502,7 @@ class RouteMixin:
         name: Optional[str] = None,
         ignore_body: bool = True,
         version_prefix: str = "/v",
+        error_format: Optional[str] = None,
     ) -> RouteWrapper:
         """
         Add an API URL under the **DELETE** *HTTP* method
@@ -502,6 +526,7 @@ class RouteMixin:
             name=name,
             ignore_body=ignore_body,
             version_prefix=version_prefix,
+            error_format=error_format,
         )
 
     def websocket(
@@ -514,6 +539,7 @@ class RouteMixin:
         name: Optional[str] = None,
         apply: bool = True,
         version_prefix: str = "/v",
+        error_format: Optional[str] = None,
     ):
         """
         Decorate a function to be registered as a websocket route
@@ -540,6 +566,7 @@ class RouteMixin:
             subprotocols=subprotocols,
             websocket=True,
             version_prefix=version_prefix,
+            error_format=error_format,
         )
 
     def add_websocket_route(
@@ -552,6 +579,7 @@ class RouteMixin:
         version: Optional[int] = None,
         name: Optional[str] = None,
         version_prefix: str = "/v",
+        error_format: Optional[str] = None,
     ):
         """
         A helper method to register a function as a websocket route.
@@ -580,6 +608,7 @@ class RouteMixin:
             version=version,
             name=name,
             version_prefix=version_prefix,
+            error_format=error_format,
         )(handler)
 
     def static(
@@ -789,8 +818,8 @@ class RouteMixin:
             )
         except Exception:
             error_logger.exception(
-                f"Exception in static request handler:\
- path={file_or_directory}, "
+                f"Exception in static request handler: "
+                f"path={file_or_directory}, "
                 f"relative_url={__file_uri__}"
             )
             raise
@@ -888,3 +917,43 @@ class RouteMixin:
         )(_handler)
 
         return route
+
+    def _determine_error_format(self, handler) -> str:
+        if not isinstance(handler, CompositionView):
+            try:
+                src = dedent(getsource(handler))
+                tree = parse(src)
+                http_response_types = self._get_response_types(tree)
+
+                if len(http_response_types) == 1:
+                    return next(iter(http_response_types))
+            except OSError:
+                ...
+
+        return "auto"
+
+    def _get_response_types(self, node):
+        types = set()
+
+        class HttpResponseVisitor(NodeVisitor):
+            def visit_Return(self, node: Return) -> Any:
+                nonlocal types
+
+                try:
+                    checks = [node.value.func.id]  # type: ignore
+                    if node.value.keywords:  # type: ignore
+                        checks += [
+                            k.value
+                            for k in node.value.keywords  # type: ignore
+                            if k.arg == "content_type"
+                        ]
+
+                    for check in checks:
+                        if check in RESPONSE_MAPPING:
+                            types.add(RESPONSE_MAPPING[check])
+                except AttributeError:
+                    ...
+
+        HttpResponseVisitor().visit(node)
+
+        return types
diff --git a/sanic/models/futures.py b/sanic/models/futures.py
index 8fd21655..fe7d77eb 100644
--- a/sanic/models/futures.py
+++ b/sanic/models/futures.py
@@ -24,6 +24,7 @@ class FutureRoute(NamedTuple):
     unquote: bool
     static: bool
     version_prefix: str
+    error_format: Optional[str]
 
 
 class FutureListener(NamedTuple):
diff --git a/sanic/request.py b/sanic/request.py
index 7f94de2d..c744e3c3 100644
--- a/sanic/request.py
+++ b/sanic/request.py
@@ -34,7 +34,7 @@ from sanic.compat import CancelledErrors, Header
 from sanic.constants import DEFAULT_HTTP_CONTENT_TYPE
 from sanic.exceptions import InvalidUsage
 from sanic.headers import (
-    Accept,
+    AcceptContainer,
     Options,
     parse_accept,
     parse_content_header,
@@ -139,7 +139,7 @@ class Request:
         self.conn_info: Optional[ConnInfo] = None
         self.ctx = SimpleNamespace()
         self.parsed_forwarded: Optional[Options] = None
-        self.parsed_accept: Optional[List[Accept]] = None
+        self.parsed_accept: Optional[AcceptContainer] = None
         self.parsed_json = None
         self.parsed_form = None
         self.parsed_files = None
@@ -301,7 +301,7 @@ class Request:
         return self.parsed_json
 
     @property
-    def accept(self) -> List[Accept]:
+    def accept(self) -> AcceptContainer:
         if self.parsed_accept is None:
             accept_header = self.headers.getone("accept", "")
             self.parsed_accept = parse_accept(accept_header)
diff --git a/sanic/router.py b/sanic/router.py
index 2661acf5..6995ed6d 100644
--- a/sanic/router.py
+++ b/sanic/router.py
@@ -13,6 +13,7 @@ from sanic_routing.exceptions import (
 from sanic_routing.route import Route  # type: ignore
 
 from sanic.constants import HTTP_METHODS
+from sanic.errorpages import check_error_format
 from sanic.exceptions import MethodNotSupported, NotFound, SanicException
 from sanic.models.handler_types import RouteHandler
 
@@ -78,6 +79,7 @@ class Router(BaseRouter):
         unquote: bool = False,
         static: bool = False,
         version_prefix: str = "/v",
+        error_format: Optional[str] = None,
     ) -> Union[Route, List[Route]]:
         """
         Add a handler to the router
@@ -137,6 +139,11 @@ class Router(BaseRouter):
             route.ctx.stream = stream
             route.ctx.hosts = hosts
             route.ctx.static = static
+            route.ctx.error_format = (
+                error_format or self.ctx.app.config.FALLBACK_ERROR_FORMAT
+            )
+
+            check_error_format(route.ctx.error_format)
 
             routes.append(route)
 
diff --git a/tests/conftest.py b/tests/conftest.py
index d24066c5..175e967e 100644
--- a/tests/conftest.py
+++ b/tests/conftest.py
@@ -109,6 +109,7 @@ def sanic_router(app):
     # noinspection PyProtectedMember
     def _setup(route_details: tuple) -> Tuple[Router, tuple]:
         router = Router()
+        router.ctx.app = app
         added_router = []
         for method, route in route_details:
             try:
diff --git a/tests/test_bad_request.py b/tests/test_bad_request.py
index 140fbe8a..7a87d919 100644
--- a/tests/test_bad_request.py
+++ b/tests/test_bad_request.py
@@ -20,4 +20,4 @@ def test_bad_request_response(app):
 
     app.run(host="127.0.0.1", port=42101, debug=False)
     assert lines[0] == b"HTTP/1.1 400 Bad Request\r\n"
-    assert b"Bad Request" in lines[-1]
+    assert b"Bad Request" in lines[-2]
diff --git a/tests/test_blueprint_group.py b/tests/test_blueprint_group.py
index 45e968b5..09729c15 100644
--- a/tests/test_blueprint_group.py
+++ b/tests/test_blueprint_group.py
@@ -3,7 +3,12 @@ from pytest import raises
 from sanic.app import Sanic
 from sanic.blueprint_group import BlueprintGroup
 from sanic.blueprints import Blueprint
-from sanic.exceptions import Forbidden, InvalidUsage, SanicException, ServerError
+from sanic.exceptions import (
+    Forbidden,
+    InvalidUsage,
+    SanicException,
+    ServerError,
+)
 from sanic.request import Request
 from sanic.response import HTTPResponse, text
 
diff --git a/tests/test_errorpages.py b/tests/test_errorpages.py
index 495c764f..5af4ca5f 100644
--- a/tests/test_errorpages.py
+++ b/tests/test_errorpages.py
@@ -1,10 +1,10 @@
 import pytest
 
 from sanic import Sanic
-from sanic.errorpages import exception_response
-from sanic.exceptions import NotFound
+from sanic.errorpages import HTMLRenderer, exception_response
+from sanic.exceptions import NotFound, SanicException
 from sanic.request import Request
-from sanic.response import HTTPResponse
+from sanic.response import HTTPResponse, html, json, text
 
 
 @pytest.fixture
@@ -20,7 +20,7 @@ def app():
 
 @pytest.fixture
 def fake_request(app):
-    return Request(b"/foobar", {}, "1.1", "GET", None, app)
+    return Request(b"/foobar", {"accept": "*/*"}, "1.1", "GET", None, app)
 
 
 @pytest.mark.parametrize(
@@ -47,7 +47,13 @@ def test_should_return_html_valid_setting(
     try:
         raise exception("bad stuff")
     except Exception as e:
-        response = exception_response(fake_request, e, True)
+        response = exception_response(
+            fake_request,
+            e,
+            True,
+            base=HTMLRenderer,
+            fallback=fake_request.app.config.FALLBACK_ERROR_FORMAT,
+        )
 
     assert isinstance(response, HTTPResponse)
     assert response.status == status
@@ -74,13 +80,194 @@ def test_auto_fallback_with_content_type(app):
     app.config.FALLBACK_ERROR_FORMAT = "auto"
 
     _, response = app.test_client.get(
-        "/error", headers={"content-type": "application/json"}
+        "/error", headers={"content-type": "application/json", "accept": "*/*"}
     )
     assert response.status == 500
     assert response.content_type == "application/json"
 
     _, response = app.test_client.get(
-        "/error", headers={"content-type": "text/plain"}
+        "/error", headers={"content-type": "foo/bar", "accept": "*/*"}
+    )
+    assert response.status == 500
+    assert response.content_type == "text/html; charset=utf-8"
+
+
+def test_route_error_format_set_on_auto(app):
+    @app.get("/text")
+    def text_response(request):
+        return text(request.route.ctx.error_format)
+
+    @app.get("/json")
+    def json_response(request):
+        return json({"format": request.route.ctx.error_format})
+
+    @app.get("/html")
+    def html_response(request):
+        return html(request.route.ctx.error_format)
+
+    _, response = app.test_client.get("/text")
+    assert response.text == "text"
+
+    _, response = app.test_client.get("/json")
+    assert response.json["format"] == "json"
+
+    _, response = app.test_client.get("/html")
+    assert response.text == "html"
+
+
+def test_route_error_response_from_auto_route(app):
+    @app.get("/text")
+    def text_response(request):
+        raise Exception("oops")
+        return text("Never gonna see this")
+
+    @app.get("/json")
+    def json_response(request):
+        raise Exception("oops")
+        return json({"message": "Never gonna see this"})
+
+    @app.get("/html")
+    def html_response(request):
+        raise Exception("oops")
+        return html("<h1>Never gonna see this</h1>")
+
+    _, response = app.test_client.get("/text")
+    assert response.content_type == "text/plain; charset=utf-8"
+
+    _, response = app.test_client.get("/json")
+    assert response.content_type == "application/json"
+
+    _, response = app.test_client.get("/html")
+    assert response.content_type == "text/html; charset=utf-8"
+
+
+def test_route_error_response_from_explicit_format(app):
+    @app.get("/text", error_format="json")
+    def text_response(request):
+        raise Exception("oops")
+        return text("Never gonna see this")
+
+    @app.get("/json", error_format="text")
+    def json_response(request):
+        raise Exception("oops")
+        return json({"message": "Never gonna see this"})
+
+    _, response = app.test_client.get("/text")
+    assert response.content_type == "application/json"
+
+    _, response = app.test_client.get("/json")
+    assert response.content_type == "text/plain; charset=utf-8"
+
+
+def test_unknown_fallback_format(app):
+    with pytest.raises(SanicException, match="Unknown format: bad"):
+        app.config.FALLBACK_ERROR_FORMAT = "bad"
+
+
+def test_route_error_format_unknown(app):
+    with pytest.raises(SanicException, match="Unknown format: bad"):
+
+        @app.get("/text", error_format="bad")
+        def handler(request):
+            ...
+
+
+def test_fallback_with_content_type_mismatch_accept(app):
+    app.config.FALLBACK_ERROR_FORMAT = "auto"
+
+    _, response = app.test_client.get(
+        "/error",
+        headers={"content-type": "application/json", "accept": "text/plain"},
     )
     assert response.status == 500
     assert response.content_type == "text/plain; charset=utf-8"
+
+    _, response = app.test_client.get(
+        "/error",
+        headers={"content-type": "text/plain", "accept": "foo/bar"},
+    )
+    assert response.status == 500
+    assert response.content_type == "text/html; charset=utf-8"
+
+    app.router.reset()
+
+    @app.route("/alt1")
+    @app.route("/alt2", error_format="text")
+    @app.route("/alt3", error_format="html")
+    def handler(_):
+        raise Exception("problem here")
+        # Yes, we know this return value is unreachable. This is on purpose.
+        return json({})
+
+    app.router.finalize()
+
+    _, response = app.test_client.get(
+        "/alt1",
+        headers={"accept": "foo/bar"},
+    )
+    assert response.status == 500
+    assert response.content_type == "text/html; charset=utf-8"
+    _, response = app.test_client.get(
+        "/alt1",
+        headers={"accept": "foo/bar,*/*"},
+    )
+    assert response.status == 500
+    assert response.content_type == "application/json"
+
+    _, response = app.test_client.get(
+        "/alt2",
+        headers={"accept": "foo/bar"},
+    )
+    assert response.status == 500
+    assert response.content_type == "text/html; charset=utf-8"
+    _, response = app.test_client.get(
+        "/alt2",
+        headers={"accept": "foo/bar,*/*"},
+    )
+    assert response.status == 500
+    assert response.content_type == "text/plain; charset=utf-8"
+
+    _, response = app.test_client.get(
+        "/alt3",
+        headers={"accept": "foo/bar"},
+    )
+    assert response.status == 500
+    assert response.content_type == "text/html; charset=utf-8"
+
+
+@pytest.mark.parametrize(
+    "accept,content_type,expected",
+    (
+        (None, None, "text/plain; charset=utf-8"),
+        ("foo/bar", None, "text/html; charset=utf-8"),
+        ("application/json", None, "application/json"),
+        ("application/json,text/plain", None, "application/json"),
+        ("text/plain,application/json", None, "application/json"),
+        ("text/plain,foo/bar", None, "text/plain; charset=utf-8"),
+        # Following test is valid after v22.3
+        # ("text/plain,text/html", None, "text/plain; charset=utf-8"),
+        ("*/*", "foo/bar", "text/html; charset=utf-8"),
+        ("*/*", "application/json", "application/json"),
+    ),
+)
+def test_combinations_for_auto(fake_request, accept, content_type, expected):
+    if accept:
+        fake_request.headers["accept"] = accept
+    else:
+        del fake_request.headers["accept"]
+
+    if content_type:
+        fake_request.headers["content-type"] = content_type
+
+    try:
+        raise Exception("bad stuff")
+    except Exception as e:
+        response = exception_response(
+            fake_request,
+            e,
+            True,
+            base=HTMLRenderer,
+            fallback="auto",
+        )
+
+    assert response.content_type == expected
diff --git a/tests/test_exceptions_handler.py b/tests/test_exceptions_handler.py
index ba14102a..dbf9fcbb 100644
--- a/tests/test_exceptions_handler.py
+++ b/tests/test_exceptions_handler.py
@@ -1,5 +1,7 @@
 import asyncio
 
+import pytest
+
 from bs4 import BeautifulSoup
 
 from sanic import Sanic
@@ -8,9 +10,6 @@ from sanic.handlers import ErrorHandler
 from sanic.response import stream, text
 
 
-exception_handler_app = Sanic("test_exception_handler")
-
-
 async def sample_streaming_fn(response):
     await response.write("foo,")
     await asyncio.sleep(0.001)
@@ -21,107 +20,102 @@ class ErrorWithRequestCtx(ServerError):
     pass
 
 
-@exception_handler_app.route("/1")
-def handler_1(request):
-    raise InvalidUsage("OK")
+@pytest.fixture
+def exception_handler_app():
+    exception_handler_app = Sanic("test_exception_handler")
+
+    @exception_handler_app.route("/1", error_format="html")
+    def handler_1(request):
+        raise InvalidUsage("OK")
+
+    @exception_handler_app.route("/2", error_format="html")
+    def handler_2(request):
+        raise ServerError("OK")
+
+    @exception_handler_app.route("/3", error_format="html")
+    def handler_3(request):
+        raise NotFound("OK")
+
+    @exception_handler_app.route("/4", error_format="html")
+    def handler_4(request):
+        foo = bar  # noqa -- F821
+        return text(foo)
+
+    @exception_handler_app.route("/5", error_format="html")
+    def handler_5(request):
+        class CustomServerError(ServerError):
+            pass
+
+        raise CustomServerError("Custom server error")
+
+    @exception_handler_app.route("/6/<arg:int>", error_format="html")
+    def handler_6(request, arg):
+        try:
+            foo = 1 / arg
+        except Exception as e:
+            raise e from ValueError(f"{arg}")
+        return text(foo)
+
+    @exception_handler_app.route("/7", error_format="html")
+    def handler_7(request):
+        raise Forbidden("go away!")
+
+    @exception_handler_app.route("/8", error_format="html")
+    def handler_8(request):
+
+        raise ErrorWithRequestCtx("OK")
+
+    @exception_handler_app.exception(ErrorWithRequestCtx, NotFound)
+    def handler_exception_with_ctx(request, exception):
+        return text(request.ctx.middleware_ran)
+
+    @exception_handler_app.exception(ServerError)
+    def handler_exception(request, exception):
+        return text("OK")
+
+    @exception_handler_app.exception(Forbidden)
+    async def async_handler_exception(request, exception):
+        return stream(
+            sample_streaming_fn,
+            content_type="text/csv",
+        )
+
+    @exception_handler_app.middleware
+    async def some_request_middleware(request):
+        request.ctx.middleware_ran = "Done."
+
+    return exception_handler_app
 
 
-@exception_handler_app.route("/2")
-def handler_2(request):
-    raise ServerError("OK")
-
-
-@exception_handler_app.route("/3")
-def handler_3(request):
-    raise NotFound("OK")
-
-
-@exception_handler_app.route("/4")
-def handler_4(request):
-    foo = bar  # noqa -- F821 undefined name 'bar' is done to throw exception
-    return text(foo)
-
-
-@exception_handler_app.route("/5")
-def handler_5(request):
-    class CustomServerError(ServerError):
-        pass
-
-    raise CustomServerError("Custom server error")
-
-
-@exception_handler_app.route("/6/<arg:int>")
-def handler_6(request, arg):
-    try:
-        foo = 1 / arg
-    except Exception as e:
-        raise e from ValueError(f"{arg}")
-    return text(foo)
-
-
-@exception_handler_app.route("/7")
-def handler_7(request):
-    raise Forbidden("go away!")
-
-
-@exception_handler_app.route("/8")
-def handler_8(request):
-
-    raise ErrorWithRequestCtx("OK")
-
-
-@exception_handler_app.exception(ErrorWithRequestCtx, NotFound)
-def handler_exception_with_ctx(request, exception):
-    return text(request.ctx.middleware_ran)
-
-
-@exception_handler_app.exception(ServerError)
-def handler_exception(request, exception):
-    return text("OK")
-
-
-@exception_handler_app.exception(Forbidden)
-async def async_handler_exception(request, exception):
-    return stream(
-        sample_streaming_fn,
-        content_type="text/csv",
-    )
-
-
-@exception_handler_app.middleware
-async def some_request_middleware(request):
-    request.ctx.middleware_ran = "Done."
-
-
-def test_invalid_usage_exception_handler():
+def test_invalid_usage_exception_handler(exception_handler_app):
     request, response = exception_handler_app.test_client.get("/1")
     assert response.status == 400
 
 
-def test_server_error_exception_handler():
+def test_server_error_exception_handler(exception_handler_app):
     request, response = exception_handler_app.test_client.get("/2")
     assert response.status == 200
     assert response.text == "OK"
 
 
-def test_not_found_exception_handler():
+def test_not_found_exception_handler(exception_handler_app):
     request, response = exception_handler_app.test_client.get("/3")
     assert response.status == 200
 
 
-def test_text_exception__handler():
+def test_text_exception__handler(exception_handler_app):
     request, response = exception_handler_app.test_client.get("/random")
     assert response.status == 200
     assert response.text == "Done."
 
 
-def test_async_exception_handler():
+def test_async_exception_handler(exception_handler_app):
     request, response = exception_handler_app.test_client.get("/7")
     assert response.status == 200
     assert response.text == "foo,bar"
 
 
-def test_html_traceback_output_in_debug_mode():
+def test_html_traceback_output_in_debug_mode(exception_handler_app):
     request, response = exception_handler_app.test_client.get("/4", debug=True)
     assert response.status == 500
     soup = BeautifulSoup(response.body, "html.parser")
@@ -136,12 +130,12 @@ def test_html_traceback_output_in_debug_mode():
     ) == summary_text
 
 
-def test_inherited_exception_handler():
+def test_inherited_exception_handler(exception_handler_app):
     request, response = exception_handler_app.test_client.get("/5")
     assert response.status == 200
 
 
-def test_chained_exception_handler():
+def test_chained_exception_handler(exception_handler_app):
     request, response = exception_handler_app.test_client.get(
         "/6/0", debug=True
     )
@@ -153,7 +147,6 @@ def test_chained_exception_handler():
     assert "handler_6" in html
     assert "foo = 1 / arg" in html
     assert "ValueError" in html
-    assert "The above exception was the direct cause" in html
 
     summary_text = " ".join(soup.select(".summary")[0].text.split())
     assert (
@@ -161,7 +154,7 @@ def test_chained_exception_handler():
     ) == summary_text
 
 
-def test_exception_handler_lookup():
+def test_exception_handler_lookup(exception_handler_app):
     class CustomError(Exception):
         pass
 
@@ -184,7 +177,7 @@ def test_exception_handler_lookup():
         class ModuleNotFoundError(ImportError):
             pass
 
-    handler = ErrorHandler()
+    handler = ErrorHandler("auto")
     handler.add(ImportError, import_error_handler)
     handler.add(CustomError, custom_error_handler)
     handler.add(ServerError, server_error_handler)
@@ -209,7 +202,7 @@ def test_exception_handler_lookup():
     )
 
 
-def test_exception_handler_processed_request_middleware():
+def test_exception_handler_processed_request_middleware(exception_handler_app):
     request, response = exception_handler_app.test_client.get("/8")
     assert response.status == 200
     assert response.text == "Done."
diff --git a/tests/test_headers.py b/tests/test_headers.py
index 928847e0..115bed86 100644
--- a/tests/test_headers.py
+++ b/tests/test_headers.py
@@ -5,6 +5,7 @@ import pytest
 from sanic import headers, text
 from sanic.exceptions import InvalidHeader, PayloadTooLarge
 from sanic.http import Http
+from sanic.request import Request
 
 
 @pytest.fixture
@@ -338,3 +339,31 @@ def test_value_in_accept(value):
     assert "foo/bar" in acceptable
     assert "foo/*" in acceptable
     assert "*/*" in acceptable
+
+
+@pytest.mark.parametrize("value", ("foo/bar", "foo/*"))
+def test_value_not_in_accept(value):
+    acceptable = headers.parse_accept(value)
+    assert "no/match" not in acceptable
+    assert "no/*" not in acceptable
+
+
+@pytest.mark.parametrize(
+    "header,expected",
+    (
+        (
+            "text/html,application/xhtml+xml,application/xml;q=0.9,image/avif,image/webp,*/*;q=0.8",  # noqa: E501
+            [
+                "text/html",
+                "application/xhtml+xml",
+                "image/avif",
+                "image/webp",
+                "application/xml;q=0.9",
+                "*/*;q=0.8",
+            ],
+        ),
+    ),
+)
+def test_browser_headers(header, expected):
+    request = Request(b"/", {"accept": header}, "1.1", "GET", None, None)
+    assert request.accept == expected