diff --git a/readthedocs/core/views/__init__.py b/readthedocs/core/views/__init__.py
index cc05c6541df..091c056cc26 100644
--- a/readthedocs/core/views/__init__.py
+++ b/readthedocs/core/views/__init__.py
@@ -93,6 +93,8 @@ class ErrorView(TemplateView):
     multiple subpaths for errors, as we need to show application themed errors
     for dashboard users and minimal error pages for documentation readers.
 
+    Template resolution also uses fallback to generic 4xx/5xx error templates.
+
     View arguments:
 
     status_code
@@ -105,33 +107,31 @@ class ErrorView(TemplateView):
         separate path from Proxito error templates.
     """
 
-    base_path = "errors/dashboard/"
-    status_code = 500
+    base_path = "errors/dashboard"
+    status_code = None
+    template_name = None
 
     def get_status_code(self):
-        status_code = self.status_code
-        try:
-            status_code = int(self.kwargs["status_code"])
-        except (ValueError, KeyError):
-            pass
-        return status_code
+        return self.kwargs.get("status_code", self.status_code)
+
+    def get_template_name(self):
+        return self.kwargs.get("template_name", self.template_name)
 
     def get_template_names(self):
-        status_code = self.get_status_code()
-        if settings.RTD_EXT_THEME_ENABLED:
-            # First try to load the template for the specific HTTP status code
-            # and fall back to a generic 400/500 level error template
-            status_code_class = int(status_code / 100)
-            generic_code = f"{status_code_class}xx"
-            return [
-                f"{self.base_path}/{code}.html" for code in [status_code, generic_code]
-            ]
-        # TODO the legacy dashboard has top level path errors, as is the
-        # default. This can be removed later.
-        return f"{status_code}.html"
+        template_names = []
+        if (template_name := self.get_template_name()) is not None:
+            template_names.append(template_name.rstrip("/"))
+        if (status_code := self.get_status_code()) is not None:
+            template_names.append(str(status_code))
+        return [f"{self.base_path}/{file}.html" for file in template_names]
+
+    def get_context_data(self, **kwargs):
+        context_data = super().get_context_data(**kwargs)
+        context_data["status_code"] = self.get_status_code()
+        return context_data
 
     def dispatch(self, request, *args, **kwargs):
-        context = self.get_context_data(**kwargs)
+        context = self.get_context_data()
         status_code = self.get_status_code()
         return self.render_to_response(
             context,
@@ -139,15 +139,6 @@ def dispatch(self, request, *args, **kwargs):
         )
 
 
-# TODO replace this with ErrorView and a template in `errors/` instead
-class TeapotView(TemplateView):
-    template_name = "core/teapot.html"
-
-    def get(self, request, *args, **kwargs):
-        context = self.get_context_data(**kwargs)
-        return self.render_to_response(context, status=418)
-
-
 class PageNotFoundView(View):
 
     """Just a 404 view that ignores all URL parameters."""
diff --git a/readthedocs/projects/views/base.py b/readthedocs/projects/views/base.py
index 6ddd6e9fd75..f0a092cc08c 100644
--- a/readthedocs/projects/views/base.py
+++ b/readthedocs/projects/views/base.py
@@ -107,9 +107,7 @@ def get(self, request, *args, **kwargs):
             )
 
             if is_show_dashboard_denied(self.get_project()):
-                template_name = "spam.html"
-                if settings.RTD_EXT_THEME_ENABLED:
-                    template_name = "errors/dashboard/410.html"
+                template_name = "errors/dashboard/spam.html"
                 return render(request, template_name=template_name, status=410)
 
         return super().get(request, *args, **kwargs)
diff --git a/readthedocs/proxito/exceptions.py b/readthedocs/proxito/exceptions.py
index 813037be633..6446c567bc9 100644
--- a/readthedocs/proxito/exceptions.py
+++ b/readthedocs/proxito/exceptions.py
@@ -19,7 +19,7 @@ class ContextualizedHttp404(Http404):
     The contextualized exception is handled by proxito's 404 handler
     """
 
-    template_name = "errors/404/base.html"
+    template_name = "errors/proxito/404/base.html"
     not_found_subject = pgettext_lazy(_not_found_subject_translation_context, "page")
 
     def __init__(self, http_status=404, path_not_found=None, **kwargs):
@@ -48,10 +48,8 @@ class DomainDNSHttp404(ContextualizedHttp404):
 
     """Raised if a DNS record points to us and we don't know the domain."""
 
-    template_name = "errors/404/dns.html"
-    not_found_subject = pgettext_lazy(
-        _not_found_subject_translation_context, "matching DNS record"
-    )
+    template_name = "errors/proxito/404/dns.html"
+    not_found_subject = pgettext_lazy(_not_found_subject_translation_context, "domain")
 
     def __init__(self, domain, **kwargs):
         """
@@ -73,7 +71,7 @@ class ProjectHttp404(ContextualizedHttp404):
     It indicates a number of reasons for the user.
     """
 
-    template_name = "errors/404/no_project.html"
+    template_name = "errors/proxito/404/no_project.html"
     not_found_subject = pgettext_lazy(_not_found_subject_translation_context, "project")
 
     def __init__(self, domain, **kwargs):
@@ -91,7 +89,7 @@ class SubprojectHttp404(ContextualizedHttp404):
 
     """Raised if a subproject was not found."""
 
-    template_name = "errors/404/no_subproject.html"
+    template_name = "errors/proxito/404/no_subproject.html"
     not_found_subject = pgettext_lazy(
         "Names an object not found in a 404 error", "subproject"
     )
@@ -111,7 +109,7 @@ class ProjectFilenameHttp404(ContextualizedHttp404):
 
     """Raised if a page inside an existing project was not found."""
 
-    template_name = "errors/404/no_project_page.html"
+    template_name = "errors/proxito/404/no_project_page.html"
     not_found_subject = pgettext_lazy(
         _not_found_subject_translation_context, "documentation page"
     )
@@ -136,7 +134,7 @@ class ProjectTranslationHttp404(ContextualizedHttp404):
     If a page isn't found, raise a ProjectPageHttp404.
     """
 
-    template_name = "errors/404/no_language.html"
+    template_name = "errors/proxito/404/no_language.html"
     not_found_subject = pgettext_lazy(
         "Names an object not found in a 404 error", "translation"
     )
@@ -160,7 +158,7 @@ class ProjectVersionHttp404(ContextualizedHttp404):
     Note: The containing project can be a subproject.
     """
 
-    template_name = "errors/404/no_version.html"
+    template_name = "errors/proxito/404/no_version.html"
     not_found_subject = pgettext_lazy(
         _not_found_subject_translation_context, "documentation version"
     )
diff --git a/readthedocs/proxito/urls.py b/readthedocs/proxito/urls.py
index c28cee7edea..b5093015183 100644
--- a/readthedocs/proxito/urls.py
+++ b/readthedocs/proxito/urls.py
@@ -33,12 +33,14 @@
 pip.rtd.io/_/api/*
 """
 
+from functools import reduce
+from operator import add
+
 from django.conf import settings
 from django.urls import include, path, re_path
-from django.views import defaults
 
 from readthedocs.constants import pattern_opts
-from readthedocs.core.views import HealthCheckView, TeapotView
+from readthedocs.core.views import HealthCheckView
 from readthedocs.projects.views.public import ProjectDownloadMedia
 from readthedocs.proxito.views.hosting import ReadTheDocsConfigJson
 from readthedocs.proxito.views.serve import (
@@ -49,7 +51,7 @@
     ServeSitemapXML,
     ServeStaticFiles,
 )
-from readthedocs.proxito.views.utils import proxito_404_page_handler
+from readthedocs.proxito.views.utils import ProxitoErrorView, proxito_404_page_handler
 
 DOC_PATH_PREFIX = getattr(settings, "DOC_PATH_PREFIX", "")
 
@@ -154,19 +156,19 @@
     # /projects/<project_slug>/
     re_path(
         r"^projects/(?P<project_slug>{project_slug})/$".format(**pattern_opts),
-        TeapotView.as_view(),
+        ProxitoErrorView.as_view(status_code=418),
         name="projects_detail",
     ),
     # /projects/<project_slug>/builds/
     re_path(
         (r"^projects/(?P<project_slug>{project_slug})/builds/$".format(**pattern_opts)),
-        TeapotView.as_view(),
+        ProxitoErrorView.as_view(status_code=418),
         name="builds_project_list",
     ),
     # /projects/<project_slug>/versions/
     re_path(
         r"^projects/(?P<project_slug>{project_slug})/versions/$".format(**pattern_opts),
-        TeapotView.as_view(),
+        ProxitoErrorView.as_view(status_code=418),
         name="project_version_list",
     ),
     # /projects/<project_slug>/downloads/
@@ -176,7 +178,7 @@
                 **pattern_opts
             )
         ),
-        TeapotView.as_view(),
+        ProxitoErrorView.as_view(status_code=418),
         name="project_downloads",
     ),
     # /projects/<project_slug>/builds/<build_id>/
@@ -186,21 +188,41 @@
                 **pattern_opts
             )
         ),
-        TeapotView.as_view(),
+        ProxitoErrorView.as_view(status_code=418),
         name="builds_detail",
     ),
     # /projects/<project_slug>/version/<version_slug>/
     re_path(
         r"^projects/(?P<project_slug>[-\w]+)/version/(?P<version_slug>[^/]+)/edit/$",
-        TeapotView.as_view(),
+        ProxitoErrorView.as_view(status_code=418),
         name="project_version_detail",
     ),
 ]
 
-urlpatterns = (
-    health_check_urls + proxied_urls + core_urls + docs_urls + dummy_dashboard_urls
-)
+debug_urls = [
+    # For testing error responses and templates
+    re_path(
+        r"^{DOC_PATH_PREFIX}error/(?P<template_name>.*)$".format(
+            DOC_PATH_PREFIX=DOC_PATH_PREFIX,
+        ),
+        ProxitoErrorView.as_view(),
+    ),
+]
+
+groups = [
+    health_check_urls,
+    proxied_urls,
+    core_urls,
+    docs_urls,
+    # Fallback paths only required for resolving URLs, evaluate these last
+    dummy_dashboard_urls,
+]
+
+if settings.SHOW_DEBUG_TOOLBAR:
+    groups.insert(0, debug_urls)
+
+urlpatterns = reduce(add, groups)
 
 # Use Django default error handlers to make things simpler
 handler404 = proxito_404_page_handler
-handler500 = defaults.server_error
+handler500 = ProxitoErrorView.as_view(status_code=500)
diff --git a/readthedocs/proxito/views/mixins.py b/readthedocs/proxito/views/mixins.py
index 0b014115275..600556936c0 100644
--- a/readthedocs/proxito/views/mixins.py
+++ b/readthedocs/proxito/views/mixins.py
@@ -272,7 +272,9 @@ def _spam_response(self, request, project):
             from readthedocsext.spamfighting.utils import is_serve_docs_denied  # noqa
 
             if is_serve_docs_denied(project):
-                return render(request, template_name="spam.html", status=410)
+                return render(
+                    request, template_name="errors/proxito/spam.html", status=410
+                )
 
 
 class ServeRedirectMixin:
diff --git a/readthedocs/proxito/views/utils.py b/readthedocs/proxito/views/utils.py
index c33a76a3833..527e3341377 100644
--- a/readthedocs/proxito/views/utils.py
+++ b/readthedocs/proxito/views/utils.py
@@ -2,11 +2,17 @@
 from django.http import HttpResponse
 from django.shortcuts import render
 
+from readthedocs.core.views import ErrorView
+
 from ..exceptions import ContextualizedHttp404
 
 log = structlog.get_logger(__name__)  # noqa
 
 
+class ProxitoErrorView(ErrorView):
+    base_path = "errors/proxito"
+
+
 def fast_404(request, *args, **kwargs):
     """
     A fast error page handler.
@@ -18,7 +24,7 @@ def fast_404(request, *args, **kwargs):
 
 
 def proxito_404_page_handler(
-    request, template_name="errors/404/base.html", exception=None
+    request, template_name="errors/proxito/404/base.html", exception=None
 ):
     """
     Serves a 404 error message, handling 404 exception types raised throughout the app.
diff --git a/readthedocs/templates/404.html b/readthedocs/templates/404.html
deleted file mode 100644
index 81bb1261bc4..00000000000
--- a/readthedocs/templates/404.html
+++ /dev/null
@@ -1,2 +0,0 @@
-{% extends "errors/404/base.html" %}
-{# this is the default template, used by Django's default 404 handler. Proxito has its own 404 view, but the main application doesn't (yet) #}
diff --git a/readthedocs/templates/errors/404/no_language.html b/readthedocs/templates/errors/404/no_language.html
deleted file mode 100644
index 015a9397d5d..00000000000
--- a/readthedocs/templates/errors/404/no_language.html
+++ /dev/null
@@ -1,10 +0,0 @@
-{% extends "errors/404/base.html" %}
-{% load i18n %}
-
-{# project exists but not in the requested language #}
-
-{% block 404_error_message %}
-  {% include "errors/404/include_error_message.html" %}
-  {% include "errors/404/include_search.html" with search_project=project.slug %}
-  {% include "errors/404/include_tips.html" %}
-{% endblock %}
diff --git a/readthedocs/templates/errors/404/no_project_page.html b/readthedocs/templates/errors/404/no_project_page.html
deleted file mode 100644
index 4b10444fd8d..00000000000
--- a/readthedocs/templates/errors/404/no_project_page.html
+++ /dev/null
@@ -1,10 +0,0 @@
-{% extends "errors/404/base.html" %}
-{% load i18n %}
-
-{# project exists but page doesn't #}
-
-{% block 404_error_message %}
-  {% include "errors/404/include_error_message.html" %}
-  {% include "errors/404/include_search.html" with search_project=project.slug %}
-  {% include "errors/404/include_tips.html" %}
-{% endblock %}
diff --git a/readthedocs/templates/errors/404/no_subproject.html b/readthedocs/templates/errors/404/no_subproject.html
deleted file mode 100644
index 6958f403e13..00000000000
--- a/readthedocs/templates/errors/404/no_subproject.html
+++ /dev/null
@@ -1,10 +0,0 @@
-{% extends "errors/404/base.html" %}
-{% load i18n %}
-
-{# project exists but subproject doesn't #}
-
-{% block 404_error_message %}
-  {% include "errors/404/include_error_message.html" %}
-  {% include "errors/404/include_search.html" with search_project=project.slug %}
-  {% include "errors/404/include_tips.html" %}
-{% endblock %}
diff --git a/readthedocs/templates/errors/404/no_version.html b/readthedocs/templates/errors/404/no_version.html
deleted file mode 100644
index 3e4d62c939d..00000000000
--- a/readthedocs/templates/errors/404/no_version.html
+++ /dev/null
@@ -1,10 +0,0 @@
-{% extends "errors/404/base.html" %}
-{% load i18n %}
-
-{# project exists but version doesn't #}
-
-{% block 404_error_message %}
-  {% include "errors/404/include_error_message.html" %}
-  {% include "errors/404/include_search.html" with search_project=project.slug %}
-  {% include "errors/404/include_tips.html" %}
-{% endblock %}
diff --git a/readthedocs/templates/401.html b/readthedocs/templates/errors/dashboard/401.html
similarity index 87%
rename from readthedocs/templates/401.html
rename to readthedocs/templates/errors/dashboard/401.html
index b5db786a6df..c50f8a26c6c 100644
--- a/readthedocs/templates/401.html
+++ b/readthedocs/templates/errors/dashboard/401.html
@@ -1,4 +1,4 @@
-{% extends "errors/base.html" %}
+{% extends "errors/dashboard/base.html" %}
 {% load core_tags %}
 {% load i18n %}
 
diff --git a/readthedocs/templates/403.html b/readthedocs/templates/errors/dashboard/403.html
similarity index 100%
rename from readthedocs/templates/403.html
rename to readthedocs/templates/errors/dashboard/403.html
diff --git a/readthedocs/templates/errors/dashboard/404.html b/readthedocs/templates/errors/dashboard/404.html
new file mode 100644
index 00000000000..7b83c17302a
--- /dev/null
+++ b/readthedocs/templates/errors/dashboard/404.html
@@ -0,0 +1,46 @@
+{% extends "errors/dashboard/base.html" %}
+{% load core_tags %}
+{% load i18n %}
+
+{% block title %}
+  {% trans "404 Not Found" %}
+{% endblock %}
+
+{% block content %}
+
+<h1>{% trans "404 Not Found" %}</h1>
+
+  {% block 404_error_message %}
+<section>
+  <p>{% trans "You have encountered a 404 on Read the Docs. You are either looking for a page that does not exist or a project that has been removed." %}</p>
+</section>
+
+<pre style="line-height: 1.25; white-space: pre;">
+
+        \       What a maze!        /
+         \                         /
+          \    This page does     /
+           ]     not exist.      [    ,'|
+           ]                     [   /  |
+           ]___               ___[ ,'   |
+           ]  ]\             /[  [ |:   |
+           ]  ] \           / [  [ |:   |
+           ]  ]  ]         [  [  [ |:   |
+           ]  ]  ]__     __[  [  [ |:   |
+           ]  ]  ] ]\ _ /[ [  [  [ |:   |
+           ]  ]  ] ] (#) [ [  [  [ :===='
+           ]  ]  ]_].nHn.[_[  [  [
+           ]  ]  ]  HHHHH. [  [  [
+           ]  ] /   `HH("N  \ [  [
+           ]__]/     HHH  "  \[__[
+           ]         NNN         [
+           ]         N/"         [
+           ]         N H         [
+          /          N            \
+         /           q,            \
+        /                           \
+</pre>
+
+  {% endblock %}
+
+{% endblock %}
diff --git a/readthedocs/templates/429.html b/readthedocs/templates/errors/dashboard/429.html
similarity index 89%
rename from readthedocs/templates/429.html
rename to readthedocs/templates/errors/dashboard/429.html
index 600a2b3ff7a..aa7de6f707f 100644
--- a/readthedocs/templates/429.html
+++ b/readthedocs/templates/errors/dashboard/429.html
@@ -1,4 +1,4 @@
-{% extends "errors/base.html" %}
+{% extends "errors/dashboard/base.html" %}
 {% load core_tags %}
 {% load i18n %}
 
diff --git a/readthedocs/templates/errors/dashboard/4xx.html b/readthedocs/templates/errors/dashboard/4xx.html
new file mode 100644
index 00000000000..ea595681c2e
--- /dev/null
+++ b/readthedocs/templates/errors/dashboard/4xx.html
@@ -0,0 +1,20 @@
+{% extends "errors/dashboard/base.html" %}
+{% load core_tags %}
+{% load i18n %}
+
+{% block title %}
+  {% trans "Bad request" %}
+{% endblock %}
+
+{% block content %}
+<h3>
+  {% blocktrans trimmed %}
+    Bad request
+  {% endblocktrans %}
+</h3>
+<p>
+  {% blocktrans trimmed %}
+    Your request is either unsupported or we didn't understand it.
+  {% endblocktrans %}
+</p>
+{% endblock %}
diff --git a/readthedocs/templates/500.html b/readthedocs/templates/errors/dashboard/500.html
similarity index 88%
rename from readthedocs/templates/500.html
rename to readthedocs/templates/errors/dashboard/500.html
index 381ca625572..61e68c00247 100644
--- a/readthedocs/templates/500.html
+++ b/readthedocs/templates/errors/dashboard/500.html
@@ -1,4 +1,4 @@
-{% extends "errors/base.html" %}
+{% extends "errors/dashboard/base.html" %}
 {% load i18n %}
 
 {% block title %}
diff --git a/readthedocs/templates/errors/dashboard/5xx.html b/readthedocs/templates/errors/dashboard/5xx.html
new file mode 120000
index 00000000000..0f3fa109755
--- /dev/null
+++ b/readthedocs/templates/errors/dashboard/5xx.html
@@ -0,0 +1 @@
+500.html
\ No newline at end of file
diff --git a/readthedocs/templates/errors/dashboard/base.html b/readthedocs/templates/errors/dashboard/base.html
new file mode 100644
index 00000000000..d6dd60f4cfa
--- /dev/null
+++ b/readthedocs/templates/errors/dashboard/base.html
@@ -0,0 +1 @@
+{% extends "errors/base.html" %}
diff --git a/readthedocs/templates/spam.html b/readthedocs/templates/errors/dashboard/spam.html
similarity index 100%
rename from readthedocs/templates/spam.html
rename to readthedocs/templates/errors/dashboard/spam.html
diff --git a/readthedocs/templates/errors/proxito/401.html b/readthedocs/templates/errors/proxito/401.html
index c1da9224c41..f479f7f09fb 120000
--- a/readthedocs/templates/errors/proxito/401.html
+++ b/readthedocs/templates/errors/proxito/401.html
@@ -1 +1 @@
-../../401.html
\ No newline at end of file
+../dashboard/401.html
\ No newline at end of file
diff --git a/readthedocs/templates/errors/proxito/403.html b/readthedocs/templates/errors/proxito/403.html
new file mode 120000
index 00000000000..f479f7f09fb
--- /dev/null
+++ b/readthedocs/templates/errors/proxito/403.html
@@ -0,0 +1 @@
+../dashboard/401.html
\ No newline at end of file
diff --git a/readthedocs/templates/errors/404/base.html b/readthedocs/templates/errors/proxito/404/base.html
similarity index 96%
rename from readthedocs/templates/errors/404/base.html
rename to readthedocs/templates/errors/proxito/404/base.html
index 524fde40346..57401598fb1 100644
--- a/readthedocs/templates/errors/404/base.html
+++ b/readthedocs/templates/errors/proxito/404/base.html
@@ -1,4 +1,4 @@
-{% extends "errors/base.html" %}
+{% extends "errors/proxito/base.html" %}
 {% load core_tags %}
 {% load i18n %}
 
diff --git a/readthedocs/templates/errors/404/dns.html b/readthedocs/templates/errors/proxito/404/dns.html
similarity index 96%
rename from readthedocs/templates/errors/404/dns.html
rename to readthedocs/templates/errors/proxito/404/dns.html
index 30ce574516a..62c0670f812 100644
--- a/readthedocs/templates/errors/404/dns.html
+++ b/readthedocs/templates/errors/proxito/404/dns.html
@@ -1,4 +1,4 @@
-{% extends "errors/404/base.html" %}
+{% extends "errors/proxito/404/base.html" %}
 {% load core_tags %}
 {% load i18n %}
 
diff --git a/readthedocs/templates/errors/404/include_error_message.html b/readthedocs/templates/errors/proxito/404/include_error_message.html
similarity index 100%
rename from readthedocs/templates/errors/404/include_error_message.html
rename to readthedocs/templates/errors/proxito/404/include_error_message.html
diff --git a/readthedocs/templates/errors/404/include_search.html b/readthedocs/templates/errors/proxito/404/include_search.html
similarity index 100%
rename from readthedocs/templates/errors/404/include_search.html
rename to readthedocs/templates/errors/proxito/404/include_search.html
diff --git a/readthedocs/templates/errors/404/include_tips.html b/readthedocs/templates/errors/proxito/404/include_tips.html
similarity index 100%
rename from readthedocs/templates/errors/404/include_tips.html
rename to readthedocs/templates/errors/proxito/404/include_tips.html
diff --git a/readthedocs/templates/errors/proxito/404/no_language.html b/readthedocs/templates/errors/proxito/404/no_language.html
new file mode 100644
index 00000000000..285fe29fc0a
--- /dev/null
+++ b/readthedocs/templates/errors/proxito/404/no_language.html
@@ -0,0 +1,10 @@
+{% extends "errors/proxito/404/base.html" %}
+{% load i18n %}
+
+{# project exists but not in the requested language #}
+
+{% block 404_error_message %}
+  {% include "errors/proxito/404/include_error_message.html" %}
+  {% include "errors/proxito/404/include_search.html" with search_project=project.slug %}
+  {% include "errors/proxito/404/include_tips.html" %}
+{% endblock %}
diff --git a/readthedocs/templates/errors/404/no_project.html b/readthedocs/templates/errors/proxito/404/no_project.html
similarity index 80%
rename from readthedocs/templates/errors/404/no_project.html
rename to readthedocs/templates/errors/proxito/404/no_project.html
index 376c49d0606..e9f3d2c2743 100644
--- a/readthedocs/templates/errors/404/no_project.html
+++ b/readthedocs/templates/errors/proxito/404/no_project.html
@@ -1,4 +1,4 @@
-{% extends "errors/404/base.html" %}
+{% extends "errors/proxito/404/base.html" %}
 {% load i18n %}
 
 {# visiting a slug or subdomain that doesn't match a project #}
@@ -12,5 +12,5 @@
     </p>
   </section>
 
-  {% include "errors/404/include_search.html" %}
+  {% include "errors/proxito/404/include_search.html" %}
 {% endblock %}
diff --git a/readthedocs/templates/errors/proxito/404/no_project_page.html b/readthedocs/templates/errors/proxito/404/no_project_page.html
new file mode 100644
index 00000000000..52d6d456d96
--- /dev/null
+++ b/readthedocs/templates/errors/proxito/404/no_project_page.html
@@ -0,0 +1,10 @@
+{% extends "errors/proxito/404/base.html" %}
+{% load i18n %}
+
+{# project exists but page doesn't #}
+
+{% block 404_error_message %}
+  {% include "errors/proxito/404/include_error_message.html" %}
+  {% include "errors/proxito/404/include_search.html" with search_project=project.slug %}
+  {% include "errors/proxito/404/include_tips.html" %}
+{% endblock %}
diff --git a/readthedocs/templates/errors/proxito/404/no_subproject.html b/readthedocs/templates/errors/proxito/404/no_subproject.html
new file mode 100644
index 00000000000..82d5c7538b2
--- /dev/null
+++ b/readthedocs/templates/errors/proxito/404/no_subproject.html
@@ -0,0 +1,10 @@
+{% extends "errors/proxito/404/base.html" %}
+{% load i18n %}
+
+{# project exists but subproject doesn't #}
+
+{% block 404_error_message %}
+  {% include "errors/proxito/404/include_error_message.html" %}
+  {% include "errors/proxito/404/include_search.html" with search_project=project.slug %}
+  {% include "errors/proxito/404/include_tips.html" %}
+{% endblock %}
diff --git a/readthedocs/templates/errors/proxito/404/no_version.html b/readthedocs/templates/errors/proxito/404/no_version.html
new file mode 100644
index 00000000000..73faa38e9e5
--- /dev/null
+++ b/readthedocs/templates/errors/proxito/404/no_version.html
@@ -0,0 +1,10 @@
+{% extends "errors/proxito/404/base.html" %}
+{% load i18n %}
+
+{# project exists but version doesn't #}
+
+{% block 404_error_message %}
+  {% include "errors/proxito/404/include_error_message.html" %}
+  {% include "errors/proxito/404/include_search.html" with search_project=project.slug %}
+  {% include "errors/proxito/404/include_tips.html" %}
+{% endblock %}
diff --git a/readthedocs/templates/core/teapot.html b/readthedocs/templates/errors/proxito/418.html
similarity index 81%
rename from readthedocs/templates/core/teapot.html
rename to readthedocs/templates/errors/proxito/418.html
index c9d8ec152ff..4d5478629aa 100644
--- a/readthedocs/templates/core/teapot.html
+++ b/readthedocs/templates/errors/proxito/418.html
@@ -1,4 +1,5 @@
-{% extends "errors/base.html" %}
+{% extends "errors/proxito/4xx.html" %}
+
 {% load core_tags %}
 {% load i18n %}
 
diff --git a/readthedocs/templates/errors/proxito/429.html b/readthedocs/templates/errors/proxito/429.html
new file mode 120000
index 00000000000..94d8439a50a
--- /dev/null
+++ b/readthedocs/templates/errors/proxito/429.html
@@ -0,0 +1 @@
+../dashboard/429.html
\ No newline at end of file
diff --git a/readthedocs/templates/errors/proxito/4xx.html b/readthedocs/templates/errors/proxito/4xx.html
new file mode 100644
index 00000000000..ec09794f0d4
--- /dev/null
+++ b/readthedocs/templates/errors/proxito/4xx.html
@@ -0,0 +1,12 @@
+{% extends "errors/proxito/base.html" %}
+
+{% load core_tags %}
+{% load i18n %}
+
+{% block title %}
+  {% trans "Bad request" %}
+{% endblock %}
+
+{% block content %}
+  <h1>{% trans "Bad request" %}</h1>
+{% endblock %}
diff --git a/readthedocs/templates/errors/proxito/500.html b/readthedocs/templates/errors/proxito/500.html
new file mode 120000
index 00000000000..baae7d90a5a
--- /dev/null
+++ b/readthedocs/templates/errors/proxito/500.html
@@ -0,0 +1 @@
+../dashboard/500.html
\ No newline at end of file
diff --git a/readthedocs/templates/errors/proxito/5xx.html b/readthedocs/templates/errors/proxito/5xx.html
new file mode 120000
index 00000000000..baae7d90a5a
--- /dev/null
+++ b/readthedocs/templates/errors/proxito/5xx.html
@@ -0,0 +1 @@
+../dashboard/500.html
\ No newline at end of file
diff --git a/readthedocs/templates/errors/proxito/base.html b/readthedocs/templates/errors/proxito/base.html
new file mode 100644
index 00000000000..d6dd60f4cfa
--- /dev/null
+++ b/readthedocs/templates/errors/proxito/base.html
@@ -0,0 +1 @@
+{% extends "errors/base.html" %}
diff --git a/readthedocs/templates/errors/proxito/spam.html b/readthedocs/templates/errors/proxito/spam.html
new file mode 120000
index 00000000000..3fe7b9eac4d
--- /dev/null
+++ b/readthedocs/templates/errors/proxito/spam.html
@@ -0,0 +1 @@
+../dashboard/spam.html
\ No newline at end of file
diff --git a/readthedocs/urls.py b/readthedocs/urls.py
index 4abd1349b65..e98387db4c3 100644
--- a/readthedocs/urls.py
+++ b/readthedocs/urls.py
@@ -122,9 +122,9 @@
         TemplateView.as_view(template_name="style_catalog.html"),
     ),
     # For testing error responses and templates
-    path(
-        "error/<int:status_code>/",
-        ErrorView.as_view(base_path="errors/dashboard"),
+    re_path(
+        r"^error/(?P<template_name>.*)$",
+        ErrorView.as_view(),
     ),
     # This must come last after the build output files
     path(