diff --git a/.changeset/fetcher-404.md b/.changeset/fetcher-404.md
new file mode 100644
index 0000000000..ce885ca279
--- /dev/null
+++ b/.changeset/fetcher-404.md
@@ -0,0 +1,5 @@
+---
+"@remix-run/router": patch
+---
+
+Ensure proper 404 error on `fetcher.load` call to a route without a `loader`
diff --git a/packages/router/__tests__/router-test.ts b/packages/router/__tests__/router-test.ts
index e4c4ef412f..acd650f332 100644
--- a/packages/router/__tests__/router-test.ts
+++ b/packages/router/__tests__/router-test.ts
@@ -10279,6 +10279,150 @@ describe("a router", () => {
         await F.actions.index.resolve("INDEX ACTION");
         expect(t.router.getFetcher(key).data).toBe("INDEX ACTION");
       });
+
+      it("throws a 404 ErrorResponse without ?index and parent route has no loader", async () => {
+        let t = setup({
+          routes: [
+            {
+              id: "parent",
+              path: "parent",
+              children: [
+                {
+                  id: "index",
+                  index: true,
+                  loader: true,
+                },
+              ],
+            },
+          ],
+          initialEntries: ["/parent"],
+          hydrationData: { loaderData: { index: "INDEX" } },
+        });
+
+        let key = "KEY";
+        await t.fetch("/parent");
+        expect(t.router.state.errors).toMatchInlineSnapshot(`
+          {
+            "parent": ErrorResponse {
+              "data": "Error: No route matches URL "/parent"",
+              "error": [Error: No route matches URL "/parent"],
+              "internal": true,
+              "status": 404,
+              "statusText": "Not Found",
+            },
+          }
+        `);
+        expect(t.router.getFetcher(key).data).toBe(undefined);
+      });
+
+      it("throws a 404 ErrorResponse with ?index and index route has no loader", async () => {
+        let t = setup({
+          routes: [
+            {
+              id: "parent",
+              path: "parent",
+              loader: true,
+              children: [
+                {
+                  id: "index",
+                  index: true,
+                },
+              ],
+            },
+          ],
+          initialEntries: ["/parent"],
+          hydrationData: { loaderData: { parent: "PARENT" } },
+        });
+
+        let key = "KEY";
+        await t.fetch("/parent?index");
+        expect(t.router.state.errors).toMatchInlineSnapshot(`
+          {
+            "parent": ErrorResponse {
+              "data": "Error: No route matches URL "/parent?index"",
+              "error": [Error: No route matches URL "/parent?index"],
+              "internal": true,
+              "status": 404,
+              "statusText": "Not Found",
+            },
+          }
+        `);
+        expect(t.router.getFetcher(key).data).toBe(undefined);
+      });
+
+      it("throws a 405 ErrorResponse without ?index and parent route has no action", async () => {
+        let t = setup({
+          routes: [
+            {
+              id: "parent",
+              path: "parent",
+              children: [
+                {
+                  id: "index",
+                  index: true,
+                  action: true,
+                },
+              ],
+            },
+          ],
+          initialEntries: ["/parent"],
+        });
+
+        let key = "KEY";
+        await t.fetch("/parent", {
+          formMethod: "post",
+          formData: createFormData({}),
+        });
+        expect(t.router.state.errors).toMatchInlineSnapshot(`
+          {
+            "parent": ErrorResponse {
+              "data": "Error: You made a POST request to "/parent" but did not provide an \`action\` for route "parent", so there is no way to handle the request.",
+              "error": [Error: You made a POST request to "/parent" but did not provide an \`action\` for route "parent", so there is no way to handle the request.],
+              "internal": true,
+              "status": 405,
+              "statusText": "Method Not Allowed",
+            },
+          }
+        `);
+        expect(t.router.getFetcher(key).data).toBe(undefined);
+      });
+
+      it("throws a 405 ErrorResponse with ?index and index route has no action", async () => {
+        let t = setup({
+          routes: [
+            {
+              id: "parent",
+              path: "parent",
+              action: true,
+              children: [
+                {
+                  id: "index",
+                  index: true,
+                },
+              ],
+            },
+          ],
+          initialEntries: ["/parent"],
+        });
+
+        let key = "KEY";
+        await t.fetch("/parent?index", {
+          formMethod: "post",
+          formData: createFormData({}),
+        });
+        expect(t.router.state.errors).toMatchInlineSnapshot(`
+          {
+            "parent": ErrorResponse {
+              "data": "Error: You made a POST request to "/parent?index" but did not provide an \`action\` for route "parent", so there is no way to handle the request.",
+              "error": [Error: You made a POST request to "/parent?index" but did not provide an \`action\` for route "parent", so there is no way to handle the request.],
+              "internal": true,
+              "status": 405,
+              "statusText": "Method Not Allowed",
+            },
+          }
+        `);
+        expect(t.router.getFetcher(key).data).toBe(undefined);
+      });
     });
   });
 
@@ -15443,12 +15587,20 @@ describe("a router", () => {
       expect(currentRouter.state.loaderData).toEqual({
         root: "ROOT*",
       });
-      // Fetcher should have been revalidated but thrown an errow since the
+      // Fetcher should have been revalidated but throw an error since the
       // loader was removed
       expect(currentRouter.state.fetchers.get("key")?.data).toBe(undefined);
-      expect(currentRouter.state.errors).toEqual({
-        root: new Error('Could not find the loader to run on the "foo" route'),
-      });
+      expect(currentRouter.state.errors).toMatchInlineSnapshot(`
+        {
+          "root": ErrorResponse {
+            "data": "Error: No route matches URL "/foo"",
+            "error": [Error: No route matches URL "/foo"],
+            "internal": true,
+            "status": 404,
+            "statusText": "Not Found",
+          },
+        }
+      `);
     });
 
     it("should retain existing routes until revalidation completes on route removal (fetch)", async () => {
diff --git a/packages/router/router.ts b/packages/router/router.ts
index 3427af0149..f0b7c6c305 100644
--- a/packages/router/router.ts
+++ b/packages/router/router.ts
@@ -3425,9 +3425,11 @@ async function callLoaderOrAction(
           // previously-lazy-loaded routes
           result = await runHandler(handler);
         } else if (type === "action") {
+          let url = new URL(request.url);
+          let pathname = url.pathname + url.search;
           throw getInternalRouterError(405, {
             method: request.method,
-            pathname: new URL(request.url).pathname,
+            pathname,
             routeId: match.route.id,
           });
         } else {
@@ -3436,12 +3438,13 @@ async function callLoaderOrAction(
           return { type: ResultType.data, data: undefined };
         }
       }
+    } else if (!handler) {
+      let url = new URL(request.url);
+      let pathname = url.pathname + url.search;
+      throw getInternalRouterError(404, {
+        pathname,
+      });
     } else {
-      invariant<Function>(
-        handler,
-        `Could not find the ${type} to run on the "${match.route.id}" route`
-      );
-
       result = await runHandler(handler);
     }