diff --git a/extensions/matrix/src/matrix/sdk/transport.test.ts b/extensions/matrix/src/matrix/sdk/transport.test.ts
index 6936196ab41c..5ac0031ff038 100644
--- a/extensions/matrix/src/matrix/sdk/transport.test.ts
+++ b/extensions/matrix/src/matrix/sdk/transport.test.ts
@@ -29,6 +29,71 @@ describe("performMatrixRequest", () => {
     clearTestUndiciRuntimeDepsOverride();
   });
 
+  it.each([
+    {
+      name: "a root homeserver",
+      homeserverPath: "",
+      expectedPath: "/_matrix/client/v3/account/whoami",
+    },
+    {
+      name: "a proxy prefix without a trailing slash",
+      homeserverPath: "/matrix-proxy",
+      expectedPath: "/matrix-proxy/_matrix/client/v3/account/whoami",
+    },
+    {
+      name: "a proxy prefix with a trailing slash",
+      homeserverPath: "/matrix-proxy/",
+      expectedPath: "/matrix-proxy/_matrix/client/v3/account/whoami",
+    },
+    {
+      name: "an encoded nested proxy prefix",
+      homeserverPath: "/proxy%20base/tenant/",
+      expectedPath: "/proxy%20base/tenant/_matrix/client/v3/account/whoami",
+    },
+  ])(
+    "preserves $name through the real HTTP transport",
+    async ({ homeserverPath, expectedPath }) => {
+      const requests: Array<{ url: string | undefined; authorization: string | undefined }> = [];
+      const server = http.createServer((request, response) => {
+        requests.push({
+          url: request.url,
+          authorization: request.headers.authorization,
+        });
+        response.writeHead(200, { "content-type": "application/json" });
+        response.end(JSON.stringify({ user_id: "@bot:example.org" }));
+      });
+      await new Promise<void>((resolve) => {
+        server.listen(0, "127.0.0.1", resolve);
+      });
+      const { port } = server.address() as { port: number };
+
+      try {
+        const result = await performMatrixRequest({
+          homeserver: `http://127.0.0.1:${port}${homeserverPath}`,
+          accessToken: "test-token",
+          method: "GET",
+          endpoint: "/_matrix/client/v3/account/whoami",
+          qs: { via: "proxy path" },
+          timeoutMs: 5000,
+          ssrfPolicy: { allowPrivateNetwork: true },
+        });
+
+        expect(result.response.status).toBe(200);
+        expect(JSON.parse(result.text)).toEqual({ user_id: "@bot:example.org" });
+        expect(requests).toEqual([
+          {
+            url: `${expectedPath}?via=proxy+path`,
+            authorization: "Bearer test-token",
+          },
+        ]);
+      } finally {
+        await new Promise<void>((resolve) => {
+          server.close(() => resolve());
+        });
+      }
+    },
+  );
+
   it("rejects oversized raw responses before buffering the whole body", async () => {
     const cancel = vi.fn();
     const stream = new ReadableStream<Uint8Array>({ cancel });
diff --git a/extensions/matrix/src/matrix/sdk/transport.ts b/extensions/matrix/src/matrix/sdk/transport.ts
index 185aebc9e8bd..416641e564b4 100644
--- a/extensions/matrix/src/matrix/sdk/transport.ts
+++ b/extensions/matrix/src/matrix/sdk/transport.ts
@@ -328,7 +328,7 @@ export async function performMatrixRequest(params: {
 
   const baseUrl = isAbsoluteEndpoint
     ? new URL(params.endpoint)
-    : new URL(normalizeEndpoint(params.endpoint), params.homeserver);
+    : new URL(`${params.homeserver.replace(/\/+$/u, "")}${normalizeEndpoint(params.endpoint)}`);
   applyQuery(baseUrl, params.qs);
 
   const headers = new Headers();