diff --git a/npm-packages/convex/src/server/router.test.ts b/npm-packages/convex/src/server/router.test.ts
index 7d95902f..208d4f97 100644
--- a/npm-packages/convex/src/server/router.test.ts
+++ b/npm-packages/convex/src/server/router.test.ts
@@ -93,29 +93,45 @@ test("HttpRouter pathPrefix", () => {
     http.route({ pathPrefix: "/path1/", method: "GET", handler: action1 });
   }).toThrow();
 
-  // prefix is shadowed by prefix
-  expect(() => {
-    http.route({
-      pathPrefix: "/path1/foo/",
-      method: "GET",
-      handler: action1,
-    });
-  }).toThrow();
+  // more specific pathPrefix
+  http.route({
+    pathPrefix: "/path1/foo/",
+    method: "GET",
+    handler: action1,
+  });
 
-  // path is shadowed by prefix
-  expect(() => {
-    http.route({ path: "/path1/foo", method: "GET", handler: action1 });
-  }).toThrow();
+  // less specific pathPrefix
+  http.route({
+    pathPrefix: "/",
+    method: "GET",
+    handler: action1,
+  });
+
+  // Longest matching prefix is used.
+  expect(http.lookup("/path1/foo/bar", "GET")).toEqual([
+    action1,
+    "GET",
+    "/path1/foo/*",
+  ]);
+  expect(http.lookup("/path1/foo", "GET")).toEqual([
+    action1,
+    "GET",
+    "/path1/*",
+  ]);
+  expect(http.lookup("/path1", "GET")).toEqual([action1, "GET", "/*"]);
+
+  // Exact path is more specific than prefix
+  http.route({ path: "/path1/foo", method: "GET", handler: action1 });
+  expect(http.lookup("/path1/foo", "GET")).toEqual([
+    action1,
+    "GET",
+    "/path1/foo",
+  ]);
+  // Duplicate exact match
+  expect(() =>
+    http.route({ path: "/path1/foo", method: "GET", handler: action1 }),
+  ).toThrow();
 
   // Not shadowed: last path segment is different
   http.route({ pathPrefix: "/path11/", method: "GET", handler: action1 });
-
-  // path is shadowed by prefix
-  expect(() => {
-    http.route({
-      pathPrefix: "/path1/foo/",
-      method: "GET",
-      handler: action1,
-    });
-  }).toThrow();
 });
diff --git a/npm-packages/convex/src/server/router.ts b/npm-packages/convex/src/server/router.ts
index 29a8198e..f4b1d9ad 100644
--- a/npm-packages/convex/src/server/router.ts
+++ b/npm-packages/convex/src/server/router.ts
@@ -169,18 +169,14 @@ export class HttpRouter {
     }
 
     if ("path" in spec) {
+      if ("pathPrefix" in spec) {
+        throw new Error(
+          `Invalid httpRouter route: cannot contain both 'path' and 'pathPrefix'`,
+        );
+      }
       if (!spec.path.startsWith("/")) {
         throw new Error(`path '${spec.path}' does not start with a /`);
       }
-      const prefixes =
-        this.prefixRoutes.get(method) || new Map<string, PublicHttpAction>();
-      for (const [prefix, _] of prefixes.entries()) {
-        if (spec.path.startsWith(prefix)) {
-          throw new Error(
-            `${spec.method} path ${spec.path} is shadowed by pathPrefix ${prefix}`,
-          );
-        }
-      }
       const methods: Map<RoutableMethod, PublicHttpAction> =
         this.exactRoutes.has(spec.path)
           ? this.exactRoutes.get(spec.path)!
@@ -203,12 +199,10 @@ export class HttpRouter {
       }
       const prefixes =
         this.prefixRoutes.get(method) || new Map<string, PublicHttpAction>();
-      for (const [prefix, _] of prefixes.entries()) {
-        if (spec.pathPrefix.startsWith(prefix)) {
-          throw new Error(
-            `${spec.method} pathPrefix ${spec.pathPrefix} is shadowed by pathPrefix ${prefix}`,
-          );
-        }
+      if (prefixes.has(spec.pathPrefix)) {
+        throw new Error(
+          `${spec.method} pathPrefix ${spec.pathPrefix} is already defined`,
+        );
       }
       prefixes.set(spec.pathPrefix, handler);
       this.prefixRoutes.set(method, prefixes);
@@ -281,7 +275,10 @@ export class HttpRouter {
     if (exactMatch) return [exactMatch, method, path];
 
     const prefixes = this.prefixRoutes.get(method) || new Map();
-    for (const [pathPrefix, endpoint] of prefixes.entries()) {
+    const prefixesSorted = [...prefixes.entries()].sort(
+      ([prefixA, _a], [prefixB, _b]) => prefixB.length - prefixA.length,
+    );
+    for (const [pathPrefix, endpoint] of prefixesSorted) {
       if (path.startsWith(pathPrefix)) {
         return [endpoint, method, `${pathPrefix}*`];
       }