diff --git a/caikit_tgis_backend/tgis_backend.py b/caikit_tgis_backend/tgis_backend.py
index ad67e26..6d683f3 100644
--- a/caikit_tgis_backend/tgis_backend.py
+++ b/caikit_tgis_backend/tgis_backend.py
@@ -21,10 +21,21 @@
 # Third Party
 import grpc
 
+# Since fastapi is optional in caikit, it may not be available
+try:
+    # Third Party
+    import fastapi
+
+    HAVE_FASTAPI = True
+except ImportError:
+    HAVE_FASTAPI = False
+    fastapi = None
+
 # First Party
 from caikit.core.exceptions import error_handler
 from caikit.core.module_backends.backend_types import register_backend_type
 from caikit.core.module_backends.base import BackendBase
+from caikit.interfaces.runtime.data_model import RuntimeServerContextType
 import alog
 
 # Local
@@ -54,6 +65,10 @@ class TGISBackend(BackendBase):
     TGIS_LOCAL_GRPC_PORT = 50055
     TGIS_LOCAL_HTTP_PORT = 3000
 
+    # HTTP Header / gRPC Metadata key used to identify a route override in an
+    # inbound request context
+    ROUTE_INFO_HEADER_KEY = "x-route-info"
+
     ## Backend Interface ##
 
     backend_type = "TGIS"
@@ -164,6 +179,24 @@ def stop(self):
             log.debug("Unloading model %s on stop", model_id)
             self.unload_model(model_id)
 
+    def handle_runtime_context(
+        self,
+        model_id: str,
+        runtime_context: RuntimeServerContextType,
+    ):
+        """Handle the runtime context for a request for the given model"""
+        if route_info := self.get_route_info(runtime_context):
+            log.debug(
+                "<TGB10705560D> Registering remote model connection with context "
+                "override: 'hostname: %s'",
+                route_info,
+            )
+            self.register_model_connection(
+                model_id,
+                {"hostname": route_info},
+                fill_with_defaults=True,
+            )
+
     ## Backend user interface ##
 
     def get_connection(
@@ -312,6 +345,34 @@ def model_loaded(self) -> bool:
             self._managed_tgis is not None and self._managed_tgis.is_ready()
         )
 
+    @classmethod
+    def get_route_info(
+        cls,
+        context: Optional[RuntimeServerContextType],
+    ) -> Optional[str]:
+        """Get the string value of the x-route-info header/metadata if present
+
+        Args:
+            context (Optional[RuntimeServerContextType]): The grpc or fastapi
+                request context
+
+        Returns:
+            route_info (Optional[str]): The header/metadata value if present,
+                otherwise None
+        """
+        if context is None:
+            return context
+        if isinstance(context, grpc.ServicerContext):
+            return dict(context.invocation_metadata()).get(cls.ROUTE_INFO_HEADER_KEY)
+        if HAVE_FASTAPI and isinstance(context, fastapi.Request):
+            return context.headers.get(cls.ROUTE_INFO_HEADER_KEY)
+        error.log_raise(
+            "<TGB92615097E>",
+            TypeError(f"context is of an unsupported type: {type(context)}"),
+        )
+
+    ## Implementation Details ##
+
     def _test_connection(
         self, model_conn: Optional[TGISConnection], timeout: Optional[float] = None
     ) -> Optional[TGISConnection]:
diff --git a/tests/test_tgis_backend.py b/tests/test_tgis_backend.py
index 29cf9a7..247b790 100644
--- a/tests/test_tgis_backend.py
+++ b/tests/test_tgis_backend.py
@@ -18,13 +18,14 @@
 # Standard
 from copy import deepcopy
 from dataclasses import asdict
-from typing import Any, Dict, Optional
+from typing import Any, Dict, Optional, Union
 from unittest import mock
 import os
 import tempfile
 import time
 
 # Third Party
+import fastapi
 import grpc
 import pytest
 import tls_test_tools
@@ -96,6 +97,18 @@ def mock_tgis_fixture():
     mock_tgis.stop()
 
 
+class TestServicerContext:
+    """
+    A dummy class for mimicking ServicerContext invocation metadata storage.
+    """
+
+    def __init__(self, metadata: Dict[str, Union[str, bytes]]):
+        self.metadata = metadata
+
+    def invocation_metadata(self):
+        return list(self.metadata.items())
+
+
 ## Conn Config #################################################################
 
 
@@ -904,3 +917,74 @@ def test_tgis_backend_conn_testing_enabled(tgis_mock_insecure):
     conn = tgis_be.get_connection(model_id)
     conn.test_connection()
     conn.test_connection(timeout=1)
+
+
+@pytest.mark.parametrize(
+    argnames=["context", "route_info"],
+    argvalues=[
+        (
+            fastapi.Request(
+                {
+                    "type": "http",
+                    "headers": [
+                        (TGISBackend.ROUTE_INFO_HEADER_KEY.encode(), b"sometext")
+                    ],
+                }
+            ),
+            "sometext",
+        ),
+        (
+            fastapi.Request(
+                {"type": "http", "headers": [(b"route-info", b"sometext")]}
+            ),
+            None,
+        ),
+        (
+            TestServicerContext({TGISBackend.ROUTE_INFO_HEADER_KEY: "sometext"}),
+            "sometext",
+        ),
+        (
+            TestServicerContext({"route-info": "sometext"}),
+            None,
+        ),
+        ("should raise TypeError", None),
+        (None, None),
+        # Uncertain how to create a grpc.ServicerContext object
+    ],
+)
+def test_get_route_info(context, route_info: Optional[str]):
+    if not isinstance(context, (fastapi.Request, grpc.ServicerContext, type(None))):
+        with pytest.raises(TypeError):
+            TGISBackend.get_route_info(context)
+    else:
+        actual_route_info = TGISBackend.get_route_info(context)
+        assert actual_route_info == route_info
+
+
+def test_handle_runtime_context_with_route_info():
+    """Test that with route info present, handle_runtime_context updates the
+    model connection
+    """
+    route_info = "sometext"
+    context = fastapi.Request(
+        {
+            "type": "http",
+            "headers": [
+                (TGISBackend.ROUTE_INFO_HEADER_KEY.encode(), route_info.encode("utf-8"))
+            ],
+        }
+    )
+
+    tgis_be = TGISBackend(
+        {
+            "connection": {"hostname": "foobar:1234"},
+            "test_connections": False,
+        }
+    )
+    assert not tgis_be._model_connections
+
+    # Handle the connection and make sure model_connections is updated
+    model_id = "my-model"
+    tgis_be.handle_runtime_context(model_id, context)
+    assert model_id in tgis_be._model_connections
+    assert (conn := tgis_be.get_connection(model_id)) and conn.hostname == route_info
diff --git a/tox.ini b/tox.ini
index a94c982..ae6a5db 100644
--- a/tox.ini
+++ b/tox.ini
@@ -12,6 +12,7 @@ deps =
     grpcio-tools>=1.35.0,<2.0
     wheel>=0.38.4
     Flask>=2.2.3,<3
+    fastapi[all]>=0.100,<1
 passenv =
     LOG_LEVEL
     LOG_FILTERS