diff --git a/packages/next-swc/crates/next-api/src/app.rs b/packages/next-swc/crates/next-api/src/app.rs
index e4b2ef1d7ba21..467b1aadf34df 100644
--- a/packages/next-swc/crates/next-api/src/app.rs
+++ b/packages/next-swc/crates/next-api/src/app.rs
@@ -586,10 +586,10 @@ impl AppEndpoint {
                 .into_iter()
                 .collect(),
         };
+        let manifest_path_prefix = get_asset_prefix_from_pathname(&app_entry.pathname);
         let app_build_manifest_output = Vc::upcast(VirtualOutputAsset::new(
             node_root.join(format!(
-                "server/app{original_name}/app-build-manifest.json",
-                original_name = app_entry.original_name
+                "server/app{manifest_path_prefix}/page/app-build-manifest.json",
             )),
             AssetContent::file(
                 File::from(serde_json::to_string_pretty(&app_build_manifest)?).into(),
@@ -603,8 +603,7 @@ impl AppEndpoint {
         };
         let build_manifest_output = Vc::upcast(VirtualOutputAsset::new(
             node_root.join(format!(
-                "server/app{original_name}/build-manifest.json",
-                original_name = app_entry.original_name
+                "server/app{manifest_path_prefix}/page/build-manifest.json",
             )),
             AssetContent::file(File::from(serde_json::to_string_pretty(&build_manifest)?).into()),
         ));
@@ -623,11 +622,14 @@ impl AppEndpoint {
 
         fn create_app_paths_manifest(
             node_root: Vc<FileSystemPath>,
+            pathname: &str,
             original_name: &str,
             filename: String,
         ) -> Result<Vc<Box<dyn OutputAsset>>> {
-            let path =
-                node_root.join(format!("server/app{original_name}/app-paths-manifest.json",));
+            let manifest_path_prefix = get_asset_prefix_from_pathname(pathname);
+            let path = node_root.join(format!(
+                "server/app{manifest_path_prefix}/page/app-paths-manifest.json",
+            ));
             let app_paths_manifest = AppPathsManifest {
                 node_server_app_paths: PagesManifest {
                     pages: [(original_name.to_string(), filename)]
@@ -727,7 +729,7 @@ impl AppEndpoint {
                 let manifest_path_prefix = get_asset_prefix_from_pathname(&app_entry.pathname);
                 let middleware_manifest_v2 = Vc::upcast(VirtualOutputAsset::new(
                     node_root.join(format!(
-                        "server/app{manifest_path_prefix}/middleware-manifest.json",
+                        "server/app{manifest_path_prefix}/page/middleware-manifest.json",
                     )),
                     AssetContent::file(
                         FileContent::Content(File::from(serde_json::to_string_pretty(
@@ -739,8 +741,12 @@ impl AppEndpoint {
                 server_assets.push(middleware_manifest_v2);
 
                 // create app paths manifest
-                let app_paths_manifest_output =
-                    create_app_paths_manifest(node_root, &app_entry.original_name, base_file)?;
+                let app_paths_manifest_output = create_app_paths_manifest(
+                    node_root,
+                    &app_entry.pathname,
+                    &app_entry.original_name,
+                    base_file,
+                )?;
                 server_assets.push(app_paths_manifest_output);
 
                 AppEndpointOutput::Edge {
@@ -756,7 +762,7 @@ impl AppEndpoint {
                     .rsc_chunking_context()
                     .entry_chunk(
                         server_path.join(format!(
-                            "app/{original_name}.js",
+                            "app{original_name}.js",
                             original_name = app_entry.original_name
                         )),
                         app_entry.rsc_entry,
@@ -766,6 +772,7 @@ impl AppEndpoint {
 
                 let app_paths_manifest_output = create_app_paths_manifest(
                     node_root,
+                    &app_entry.pathname,
                     &app_entry.original_name,
                     server_path
                         .await?
diff --git a/packages/next-swc/crates/next-core/src/app_structure.rs b/packages/next-swc/crates/next-core/src/app_structure.rs
index 2f849d87eca4f..f49278c52cb69 100644
--- a/packages/next-swc/crates/next-core/src/app_structure.rs
+++ b/packages/next-swc/crates/next-core/src/app_structure.rs
@@ -804,12 +804,12 @@ async fn directory_tree_to_entrypoints_internal(
             } else {
                 format!("{path_prefix}/{subdir_name}")
             },
-            if is_route_group || parallel_route_key.is_some() {
-                path_prefix.clone()
-            } else if path_prefix == "/" {
+            if parallel_route_key.is_some() {
+                original_name_prefix.clone()
+            } else if original_name_prefix == "/" {
                 format!("/{subdir_name}")
             } else {
-                format!("{path_prefix}/{subdir_name}")
+                format!("{original_name_prefix}/{subdir_name}")
             },
         )
         .await?;
diff --git a/packages/next-swc/crates/next-core/src/next_manifests/client_reference_manifest.rs b/packages/next-swc/crates/next-core/src/next_manifests/client_reference_manifest.rs
index 078a8569d137c..4458410d02198 100644
--- a/packages/next-swc/crates/next-core/src/next_manifests/client_reference_manifest.rs
+++ b/packages/next-swc/crates/next-core/src/next_manifests/client_reference_manifest.rs
@@ -183,9 +183,9 @@ impl ClientReferenceManifest {
             AssetContent::file(
                 File::from(formatdoc! {
                     r#"
-                            globalThis.__RSC_MANIFEST = globalThis.__RSC_MANIFEST || {{}};
-                            globalThis.__RSC_MANIFEST[{entry_name}] = {manifest}
-                        "#,
+                        globalThis.__RSC_MANIFEST = globalThis.__RSC_MANIFEST || {{}};
+                        globalThis.__RSC_MANIFEST[{entry_name}] = {manifest}
+                    "#,
                     entry_name = StringifyJs(&entry_name),
                     manifest = StringifyJs(&client_reference_manifest_json)
                 })
diff --git a/packages/next/src/server/lib/router-utils/setup-dev.ts b/packages/next/src/server/lib/router-utils/setup-dev.ts
index 9f47e5caac0a6..a81d3e648ef5e 100644
--- a/packages/next/src/server/lib/router-utils/setup-dev.ts
+++ b/packages/next/src/server/lib/router-utils/setup-dev.ts
@@ -748,11 +748,9 @@ async function startWatcher(opts: SetupOpts) {
             break
           }
           case 'page-api': {
-            if (isApp) {
-              throw new Error(
-                `mis-matched route type: isApp && page for ${page}`
-              )
-            }
+            // We don't throw on ensureOpts.isApp === true here
+            // since this can happen when app pages make
+            // api requests to page API routes.
 
             const writtenEndpoint = await processResult(
               page,