diff --git a/python/lsst/daf/butler/remote_butler/_remote_butler.py b/python/lsst/daf/butler/remote_butler/_remote_butler.py
index a9a0273618..e6a1bb4429 100644
--- a/python/lsst/daf/butler/remote_butler/_remote_butler.py
+++ b/python/lsst/daf/butler/remote_butler/_remote_butler.py
@@ -33,6 +33,7 @@
 
 import httpx
 from lsst.daf.butler import __version__
+from lsst.daf.butler.repo_relocation import replaceRoot
 from lsst.resources import ResourcePath, ResourcePathExpression
 from lsst.utils.introspection import get_full_type_name
 
@@ -69,6 +70,16 @@ def __init__(
         **kwargs: Any,
     ):
         butler_config = ButlerConfig(config, searchPaths, without_datastore=True)
+        # There is a convention in Butler config files where <butlerRoot> in a
+        # configuration option refers to the directory containing the
+        # configuration file.  We allow this for the remote butler's URL so
+        # that the server doesn't have to know which hostname it is being
+        # accessed from
+        server_url_key = ("remote_butler", "url")
+        if server_url_key in butler_config:
+            butler_config[server_url_key] = replaceRoot(
+                butler_config[server_url_key], butler_config.configDir
+            )
         self._config = RemoteButlerConfigModel.model_validate(butler_config)
         self._dimensions: DimensionUniverse | None = None
         # TODO: RegistryDefaults should have finish() called on it, but this
diff --git a/python/lsst/daf/butler/remote_butler/server/_server.py b/python/lsst/daf/butler/remote_butler/server/_server.py
index 4552c541b4..64bfc5f969 100644
--- a/python/lsst/daf/butler/remote_butler/server/_server.py
+++ b/python/lsst/daf/butler/remote_butler/server/_server.py
@@ -77,6 +77,30 @@ async def get_index() -> Metadata:
     return get_metadata(package_name="lsst.daf.butler", application_name="butler")
 
 
+@app.get(
+    "/butler/butler.yaml",
+    description=(
+        "Returns a Butler YAML configuration file that can be used to instantiate a Butler client"
+        " pointing at this server"
+    ),
+    summary="Client configuration file",
+    response_model=dict[str, Any],
+)
+@app.get(
+    "/butler/butler.json",
+    description=(
+        "Returns a Butler JSON configuration file that can be used to instantiate a Butler client"
+        " pointing at this server"
+    ),
+    summary="Client configuration file",
+    response_model=dict[str, Any],
+)
+async def get_client_config() -> dict[str, Any]:
+    # We can return JSON data for both the YAML and JSON case because all JSON
+    # files are parseable as YAML.
+    return {"cls": "lsst.daf.butler.remote_butler.RemoteButler", "remote_butler": {"url": "<butlerRoot>"}}
+
+
 @app.get("/butler/v1/universe", response_model=dict[str, Any])
 def get_dimension_universe(factory: Factory = Depends(factory_dependency)) -> dict[str, Any]:
     """Allow remote client to get dimensions definition."""
diff --git a/tests/test_server.py b/tests/test_server.py
index 32c84a9c3a..622bd85954 100644
--- a/tests/test_server.py
+++ b/tests/test_server.py
@@ -37,8 +37,11 @@
     TestClient = None
     app = None
 
+from unittest.mock import patch
+
 from lsst.daf.butler import Butler
 from lsst.daf.butler.tests.utils import MetricTestRepo, makeTestTempDir, removeTestTempDir
+from lsst.resources.http import HttpResourcePath
 
 TESTDIR = os.path.abspath(os.path.dirname(__file__))
 
@@ -96,6 +99,29 @@ def test_remote_butler(self):
         universe = self.butler.dimensions
         self.assertEqual(universe.namespace, "daf_butler")
 
+    def test_instantiate_via_butler_http_search(self):
+        """Ensure that the primary Butler constructor's automatic search logic
+        correctly locates and reads the configuration file and ends up with a
+        RemoteButler pointing to the correct URL
+        """
+
+        # This is kind of a fragile test.  Butler's search logic does a lot of
+        # manipulations involving creating new ResourcePaths, and ResourcePath
+        # doesn't use httpx so we can't easily inject the TestClient in there.
+        # We don't have an actual valid HTTP URL to give to the constructor
+        # because the test instance of the server is accessed via ASGI.
+        #
+        # Instead we just monkeypatch the HTTPResourcePath 'read' method and
+        # hope that all ResourcePath HTTP reads during construction are going
+        # to the server under test.
+        def override_read(http_resource_path):
+            return self.client.get(http_resource_path.geturl()).content
+
+        with patch.object(HttpResourcePath, "read", override_read):
+            butler = Butler("https://test.example/butler")
+        assert isinstance(butler, RemoteButler)
+        assert str(butler._config.remote_butler.url) == "https://test.example/butler/"
+
 
 if __name__ == "__main__":
     unittest.main()