diff --git a/Makefile b/Makefile
index 95c69fe..745d9b9 100644
--- a/Makefile
+++ b/Makefile
@@ -6,7 +6,7 @@ BASE_PATH ?= /magic-base-path-placeholder
 
 $(CHAT_SOURCES_STAMP): $(CHAT_SOURCES)
 	@echo "Chat sources changed. Running build steps..."
-	cd chat && BASE_PATH=${BASE_PATH} bun run build
+	cd chat && NEXT_PUBLIC_BASE_PATH="${BASE_PATH}" bun run build
 	rm -rf lib/httpapi/chat && mkdir -p lib/httpapi/chat && touch lib/httpapi/chat/marker
 	cp -r chat/out/. lib/httpapi/chat/
 	touch $@
diff --git a/chat/next.config.ts b/chat/next.config.ts
index baf9e51..358d829 100644
--- a/chat/next.config.ts
+++ b/chat/next.config.ts
@@ -1,5 +1,8 @@
 import type { NextConfig } from "next";
-const basePath = process.env.BASE_PATH ?? "/chat";
+let basePath = process.env.NEXT_PUBLIC_BASE_PATH ?? "/chat";
+if (basePath.endsWith("/")) {
+  basePath = basePath.slice(0, -1);
+}
 
 const nextConfig: NextConfig = {
   // Enable static exports
diff --git a/chat/src/components/chat-provider.tsx b/chat/src/components/chat-provider.tsx
index 2d5e1e7..d57c3c8 100644
--- a/chat/src/components/chat-provider.tsx
+++ b/chat/src/components/chat-provider.tsx
@@ -51,13 +51,47 @@ interface ChatContextValue {
 
 const ChatContext = createContext<ChatContextValue | undefined>(undefined);
 
+const useAgentAPIUrl = (): string => {
+  const searchParams = useSearchParams();
+  const paramsUrl = searchParams.get("url");
+  if (paramsUrl) {
+    return paramsUrl;
+  }
+  const basePath = process.env.NEXT_PUBLIC_BASE_PATH;
+  if (!basePath) {
+    throw new Error(
+      "agentAPIUrl is not set. Please set the url query parameter to the URL of the AgentAPI or the NEXT_PUBLIC_BASE_PATH environment variable."
+    );
+  }
+  // NOTE(cian): We use '../' here to construct the agent API URL relative
+  // to the chat's location. Let's say the app is hosted on a subpath
+  // `/@admin/workspace.agent/apps/ccw/`. When you visit this URL you get
+  // redirected to `/@admin/workspace.agent/apps/ccw/chat/embed`. This serves
+  // this React application, but it needs to know where the agent API is hosted.
+  // This will be at the root of where the application is mounted e.g.
+  // `/@admin/workspace.agent/apps/ccw/`. Previously we used
+  // `window.location.origin` but this assumes that the application owns the
+  // entire origin.
+  // See: https://github.com/coder/coder/issues/18779#issuecomment-3133290494 for more context.
+  let chatURL: string = new URL(basePath, window.location.origin).toString();
+  // NOTE: trailing slashes and relative URLs are tricky.
+  // https://developer.mozilla.org/en-US/docs/Web/API/URL_API/Resolving_relative_references#current_directory_relative
+  if (!chatURL.endsWith("/")) {
+    chatURL += "/";
+  }
+  const agentAPIURL = new URL("..", chatURL).toString();
+  if (agentAPIURL.endsWith("/")) {
+    return agentAPIURL.slice(0, -1);
+  }
+  return agentAPIURL;
+};
+
 export function ChatProvider({ children }: PropsWithChildren) {
   const [messages, setMessages] = useState<(Message | DraftMessage)[]>([]);
   const [loading, setLoading] = useState<boolean>(false);
   const [serverStatus, setServerStatus] = useState<ServerStatus>("unknown");
   const eventSourceRef = useRef<EventSource | null>(null);
-  const searchParams = useSearchParams();
-  const agentAPIUrl = searchParams.get("url") || window.location.origin;
+  const agentAPIUrl = useAgentAPIUrl();
 
   // Set up SSE connection to the events endpoint
   useEffect(() => {
diff --git a/lib/httpapi/server.go b/lib/httpapi/server.go
index a343baa..3d8c710 100644
--- a/lib/httpapi/server.go
+++ b/lib/httpapi/server.go
@@ -6,6 +6,8 @@ import (
 	"fmt"
 	"log/slog"
 	"net/http"
+	"net/url"
+	"strings"
 	"sync"
 	"time"
 
@@ -33,6 +35,7 @@ type Server struct {
 	agentio      *termexec.Process
 	agentType    mf.AgentType
 	emitter      *EventEmitter
+	chatBasePath string
 }
 
 func (s *Server) GetOpenAPI() string {
@@ -95,14 +98,20 @@ func NewServer(ctx context.Context, agentType mf.AgentType, process *termexec.Pr
 		agentio:      process,
 		agentType:    agentType,
 		emitter:      emitter,
+		chatBasePath: strings.TrimSuffix(chatBasePath, "/"),
 	}
 
 	// Register API routes
-	s.registerRoutes(chatBasePath)
+	s.registerRoutes()
 
 	return s
 }
 
+// Handler returns the underlying chi.Router for testing purposes.
+func (s *Server) Handler() http.Handler {
+	return s.router
+}
+
 func (s *Server) StartSnapshotLoop(ctx context.Context) {
 	s.conversation.StartSnapshotLoop(ctx)
 	go func() {
@@ -116,7 +125,7 @@ func (s *Server) StartSnapshotLoop(ctx context.Context) {
 }
 
 // registerRoutes sets up all API endpoints
-func (s *Server) registerRoutes(chatBasePath string) {
+func (s *Server) registerRoutes() {
 	// GET /status endpoint
 	huma.Get(s.api, "/status", s.getStatus, func(o *huma.Operation) {
 		o.Description = "Returns the current status of the agent."
@@ -158,7 +167,7 @@ func (s *Server) registerRoutes(chatBasePath string) {
 	s.router.Handle("/", http.HandlerFunc(s.redirectToChat))
 
 	// Serve static files for the chat interface under /chat
-	s.registerStaticFileRoutes(chatBasePath)
+	s.registerStaticFileRoutes()
 }
 
 // getStatus handles GET /status
@@ -305,8 +314,8 @@ func (s *Server) Stop(ctx context.Context) error {
 }
 
 // registerStaticFileRoutes sets up routes for serving static files
-func (s *Server) registerStaticFileRoutes(chatBasePath string) {
-	chatHandler := FileServerWithIndexFallback(chatBasePath)
+func (s *Server) registerStaticFileRoutes() {
+	chatHandler := FileServerWithIndexFallback(s.chatBasePath)
 
 	// Mount the file server at /chat
 	s.router.Handle("/chat", http.StripPrefix("/chat", chatHandler))
@@ -314,5 +323,11 @@ func (s *Server) registerStaticFileRoutes(chatBasePath string) {
 }
 
 func (s *Server) redirectToChat(w http.ResponseWriter, r *http.Request) {
-	http.Redirect(w, r, "/chat/embed", http.StatusTemporaryRedirect)
+	rdir, err := url.JoinPath(s.chatBasePath, "embed")
+	if err != nil {
+		s.logger.Error("Failed to construct redirect URL", "error", err)
+		http.Error(w, "Failed to redirect", http.StatusInternalServerError)
+		return
+	}
+	http.Redirect(w, r, rdir, http.StatusTemporaryRedirect)
 }
diff --git a/lib/httpapi/server_test.go b/lib/httpapi/server_test.go
index 456235a..5abc5f5 100644
--- a/lib/httpapi/server_test.go
+++ b/lib/httpapi/server_test.go
@@ -6,6 +6,8 @@ import (
 	"fmt"
 	"io"
 	"log/slog"
+	"net/http"
+	"net/http/httptest"
 	"os"
 	"sort"
 	"testing"
@@ -73,3 +75,38 @@ func TestOpenAPISchema(t *testing.T) {
 
 	require.Equal(t, currentSchema, diskSchema)
 }
+
+func TestServer_redirectToChat(t *testing.T) {
+	cases := []struct {
+		name                 string
+		chatBasePath         string
+		expectedResponseCode int
+		expectedLocation     string
+	}{
+		{"default base path", "/chat", http.StatusTemporaryRedirect, "/chat/embed"},
+		{"custom base path", "/custom", http.StatusTemporaryRedirect, "/custom/embed"},
+	}
+	for _, tc := range cases {
+		t.Run(tc.name, func(t *testing.T) {
+			t.Parallel()
+			tCtx := logctx.WithLogger(context.Background(), slog.New(slog.NewTextHandler(os.Stdout, nil)))
+			s := httpapi.NewServer(tCtx, msgfmt.AgentTypeClaude, nil, 0, tc.chatBasePath)
+			tsServer := httptest.NewServer(s.Handler())
+			t.Cleanup(tsServer.Close)
+
+			client := &http.Client{
+				CheckRedirect: func(req *http.Request, via []*http.Request) error {
+					return http.ErrUseLastResponse
+				},
+			}
+			resp, err := client.Get(tsServer.URL + "/")
+			require.NoError(t, err, "unexpected error making GET request")
+			t.Cleanup(func() {
+				_ = resp.Body.Close()
+			})
+			require.Equal(t, tc.expectedResponseCode, resp.StatusCode, "expected %d status code", tc.expectedResponseCode)
+			loc := resp.Header.Get("Location")
+			require.Equal(t, tc.expectedLocation, loc, "expected Location %q, got %q", tc.expectedLocation, loc)
+		})
+	}
+}