diff --git a/superset/initialization/__init__.py b/superset/initialization/__init__.py
index e5f950fc47b..a550d11cc6c 100644
--- a/superset/initialization/__init__.py
+++ b/superset/initialization/__init__.py
@@ -464,7 +464,13 @@ class SupersetAppInitializer:  # pylint: disable=too-many-public-methods
         appbuilder.add_view_no_menu(RedirectView)
         appbuilder.add_view_no_menu(RoleRestAPI)
         appbuilder.add_view_no_menu(UserInfoView)
-        if self.config.get("FAB_API_SWAGGER_UI_SUPERSET_APP_ROOT", False):
+        # Only register the APPLICATION_ROOT-aware Swagger UI / OpenAPI spec when
+        # Swagger is enabled globally (``FAB_API_SWAGGER_UI``). This preserves the
+        # global disable contract so operators who turn Swagger off don't get the
+        # API documentation re-exposed by the prefix-aware variant.
+        if self.config.get("FAB_API_SWAGGER_UI") and self.config.get(
+            "FAB_API_SWAGGER_UI_SUPERSET_APP_ROOT", False
+        ):
             appbuilder.add_api(SupersetOpenApi)
             appbuilder.add_view_no_menu(SupersetSwaggerView)
 
@@ -915,6 +921,17 @@ class SupersetAppInitializer:  # pylint: disable=too-many-public-methods
 
         appbuilder.indexview = SupersetIndexView
         appbuilder.security_manager_class = custom_sm
+
+        # The APPLICATION_ROOT-aware Swagger UI and OpenAPI spec replace FAB's
+        # default views at the same routes (``/api/<version>/_openapi`` and
+        # ``/swagger/<version>``). Suppress FAB's default registration so the two
+        # implementations don't create duplicate URL rules for the same path,
+        # which would otherwise leave FAB's (non-prefix-aware) handler in charge.
+        if self.config.get("FAB_API_SWAGGER_UI") and self.config.get(
+            "FAB_API_SWAGGER_UI_SUPERSET_APP_ROOT", False
+        ):
+            self.superset_app.config["FAB_ADD_OPENAPI_VIEWS"] = False
+
         appbuilder.init_app(self.superset_app, db.session)
 
     def configure_url_map_converters(self) -> None:
diff --git a/superset/openapi/manager.py b/superset/openapi/manager.py
index b233a437305..7bc6a1a04db 100644
--- a/superset/openapi/manager.py
+++ b/superset/openapi/manager.py
@@ -34,6 +34,20 @@ from flask_appbuilder.security.decorators import has_access
 from superset.superset_typing import FlaskResponse
 
 
+def normalize_app_root(app_root: str | None) -> str:
+    """Normalize ``APPLICATION_ROOT`` into a prefix safe for URL concatenation.
+
+    Flask defaults ``APPLICATION_ROOT`` to ``"/"``. Concatenating that (or any
+    value with a trailing slash) directly with a leading-slash path produces an
+    invalid protocol-relative URL such as ``//api/v1/_openapi``. Treat ``"/"`` as
+    an empty prefix and strip any trailing slash so the result is either empty or
+    a clean ``/prefix``.
+    """
+    if not app_root:
+        return ""
+    return app_root.rstrip("/")
+
+
 def resolver(schema: Any) -> str:
     schema_cls = resolve_schema_cls(schema)
     name = schema_cls.__name__
@@ -86,8 +100,8 @@ class SupersetOpenApi(BaseApi):
 
     @staticmethod
     def _create_api_spec(version: str) -> APISpec:
-        app_root = current_app.config.get("APPLICATION_ROOT", "/")
-        default_server = {"url": request.host_url.rstrip("/") + app_root}
+        app_root = normalize_app_root(current_app.config.get("APPLICATION_ROOT", "/"))
+        default_server = {"url": request.host_url.rstrip("/") + (app_root or "/")}
         servers = current_app.config.get("FAB_OPENAPI_SERVERS", [default_server])
         return APISpec(
             title=current_app.appbuilder.app_name,
@@ -107,10 +121,11 @@ class SupersetSwaggerView(BaseView):
     @expose("/<version>")
     @has_access
     def show(self, version: str) -> FlaskResponse:
-        app_root = current_app.config.get("APPLICATION_ROOT", "") + self.openapi_uri
+        app_root = normalize_app_root(current_app.config.get("APPLICATION_ROOT"))
+        openapi_uri = (app_root + self.openapi_uri).format(version)
         return self.render_template(
             current_app.config.get(
                 "FAB_API_SWAGGER_TEMPLATE", "appbuilder/swagger/swagger.html"
             ),
-            openapi_uri=app_root.format(version),
+            openapi_uri=openapi_uri,
         )
diff --git a/tests/unit_tests/openapi/test_manager.py b/tests/unit_tests/openapi/test_manager.py
index 43afd54e15f..f7fbb4d4631 100644
--- a/tests/unit_tests/openapi/test_manager.py
+++ b/tests/unit_tests/openapi/test_manager.py
@@ -14,9 +14,25 @@
 # KIND, either express or implied.  See the License for the
 # specific language governing permissions and limitations
 # under the License.
+import pytest
 from marshmallow import Schema
 
-from superset.openapi.manager import resolver
+from superset.openapi.manager import normalize_app_root, resolver
+
+
+@pytest.mark.parametrize(
+    "app_root,expected",
+    [
+        ("/", ""),
+        ("", ""),
+        (None, ""),
+        ("/prefix", "/prefix"),
+        ("/prefix/", "/prefix"),
+        ("/nested/prefix/", "/nested/prefix"),
+    ],
+)
+def test_normalize_app_root(app_root: str | None, expected: str) -> None:
+    assert normalize_app_root(app_root) == expected
 
 
 def test_resolver_strips_schema_suffix() -> None: