diff --git a/readthedocs/api/v2/serializers.py b/readthedocs/api/v2/serializers.py
index 521a2e7acf4..59d09fc7530 100644
--- a/readthedocs/api/v2/serializers.py
+++ b/readthedocs/api/v2/serializers.py
@@ -17,20 +17,21 @@ class ProjectSerializer(serializers.ModelSerializer):
     class Meta:
         model = Project
         fields = (
-            'id',
-            'name',
-            'slug',
-            'description',
-            'language',
-            'programming_language',
-            'repo',
-            'repo_type',
-            'default_version',
-            'default_branch',
-            'documentation_type',
-            'users',
-            'canonical_url',
-            'urlconf',
+            "id",
+            "name",
+            "slug",
+            "description",
+            "language",
+            "programming_language",
+            "repo",
+            "repo_type",
+            "default_version",
+            "default_branch",
+            "documentation_type",
+            "users",
+            "canonical_url",
+            "urlconf",
+            "custom_prefix",
         )
 
 
diff --git a/readthedocs/projects/models.py b/readthedocs/projects/models.py
index ec4a85f248c..f5fda7a6d24 100644
--- a/readthedocs/projects/models.py
+++ b/readthedocs/projects/models.py
@@ -693,11 +693,9 @@ def proxied_api_host(self):
         This needs to start with a slash at the root of the domain,
         and end without a slash
         """
-        if self.urlconf:
-            # Add our proxied api host at the first place we have a $variable
-            # This supports both subpaths & normal root hosting
-            path_prefix = self.custom_path_prefix
-            return unsafe_join_url_path(path_prefix, "/_")
+        custom_prefix = self.proxied_api_prefix
+        if custom_prefix:
+            return unsafe_join_url_path(custom_prefix, "/_")
         return '/_'
 
     @property
@@ -715,12 +713,22 @@ def proxied_static_path(self):
         return f"{self.proxied_api_host}/static/"
 
     @property
-    def custom_path_prefix(self):
+    def proxied_api_prefix(self):
         """
-        Get the path prefix from the custom urlconf.
+        Get the path prefix for proxied API paths (``/_/``).
 
         Returns `None` if the project doesn't have a custom urlconf.
         """
+        # When using a custom prefix, we can only handle serving
+        # docs pages under the prefix, not special paths like `/_/`.
+        # Projects using the old implementation, need to proxy `/_/`
+        # paths as is, this is, without the prefix, while those projects
+        # migrate to the new implementation, we will prefix special paths
+        # when generating links, these paths will be manually un-prefixed in nginx.
+        if self.custom_prefix and self.has_feature(
+            Feature.USE_PROXIED_APIS_WITH_PREFIX
+        ):
+            return self.custom_prefix
         if self.urlconf:
             # Return the value before the first defined variable,
             # as that is a prefix and not part of our normal doc patterns.
@@ -1930,6 +1938,7 @@ def add_features(sender, **kwargs):
     DISABLE_PAGEVIEWS = "disable_pageviews"
     RESOLVE_PROJECT_FROM_HEADER = "resolve_project_from_header"
     USE_UNRESOLVER_WITH_PROXITO = "use_unresolver_with_proxito"
+    USE_PROXIED_APIS_WITH_PREFIX = "use_proxied_apis_with_prefix"
     ALLOW_VERSION_WARNING_BANNER = "allow_version_warning_banner"
 
     # Versions sync related features
@@ -2020,6 +2029,12 @@ def add_features(sender, **kwargs):
                 "Proxito: Use new unresolver implementation for serving documentation files."
             ),
         ),
+        (
+            USE_PROXIED_APIS_WITH_PREFIX,
+            _(
+                "Proxito: Use proxied APIs (/_/*) with the custom prefix if the project has one (Project.custom_prefix)."
+            ),
+        ),
         (
             ALLOW_VERSION_WARNING_BANNER,
             _("Dashboard: Allow project to use the version warning banner."),
diff --git a/readthedocs/projects/tests/test_models.py b/readthedocs/projects/tests/test_models.py
index 4e00121db45..6f6512a961f 100644
--- a/readthedocs/projects/tests/test_models.py
+++ b/readthedocs/projects/tests/test_models.py
@@ -3,7 +3,7 @@
 from django.test import TestCase
 from django_dynamic_fixture import get
 
-from readthedocs.projects.models import Project
+from readthedocs.projects.models import Feature, Project
 
 
 class TestURLPatternsUtils(TestCase):
@@ -115,3 +115,25 @@ def test_overlapping_prefixes(self):
         with pytest.raises(ValidationError) as excinfo:
             self.project.clean()
         self.assertEqual(excinfo.value.code, "ambiguous_path")
+
+    def test_proxied_api_prefix(self):
+        self.assertEqual(self.project.custom_prefix, None)
+        self.assertEqual(self.project.proxied_api_url, "_/")
+        self.assertEqual(self.project.proxied_api_host, "/_")
+        self.assertEqual(self.project.proxied_api_prefix, None)
+
+        self.project.custom_prefix = "/prefix/"
+        self.project.save()
+
+        self.assertEqual(self.project.proxied_api_url, "_/")
+        self.assertEqual(self.project.proxied_api_host, "/_")
+        self.assertEqual(self.project.proxied_api_prefix, None)
+
+        get(
+            Feature,
+            projects=[self.project],
+            feature_id=Feature.USE_PROXIED_APIS_WITH_PREFIX,
+        )
+        self.assertEqual(self.project.proxied_api_url, "prefix/_/")
+        self.assertEqual(self.project.proxied_api_host, "/prefix/_")
+        self.assertEqual(self.project.proxied_api_prefix, "/prefix/")
diff --git a/readthedocs/rtd_tests/tests/test_api.py b/readthedocs/rtd_tests/tests/test_api.py
index 5651970f569..61ea38b2366 100644
--- a/readthedocs/rtd_tests/tests/test_api.py
+++ b/readthedocs/rtd_tests/tests/test_api.py
@@ -3176,6 +3176,7 @@ def test_get_version_by_id(self):
                 "use_system_packages": False,
                 "users": [1],
                 "urlconf": None,
+                "custom_prefix": None,
             },
             "privacy_level": "public",
             "downloads": {},