diff --git a/cli/src/commands/sync/sync.ts b/cli/src/commands/sync/sync.ts
index a61cb2d60f..f139fc683e 100644
--- a/cli/src/commands/sync/sync.ts
+++ b/cli/src/commands/sync/sync.ts
@@ -91,6 +91,7 @@ import {
   isRawAppFolderMetadataFile,
   getDeleteSuffix,
   transformJsonPathToDir,
+  getFolderSuffix,
   getFolderSuffixWithSep,
 } from "../../utils/resource_folders.ts";
 
@@ -1289,7 +1290,7 @@ export async function elementsToMap(
     }
 
     if (isRawAppFile(path)) {
-      const suffix = path.split(".raw_app" + SEP).pop();
+      const suffix = path.split(getFolderSuffix("raw_app") + SEP).pop();
       if (
         suffix?.startsWith("dist/") ||
         suffix == "wmill.d.ts" ||
diff --git a/cli/src/utils/resource_folders.ts b/cli/src/utils/resource_folders.ts
index c374ad196d..8f12da2af0 100644
--- a/cli/src/utils/resource_folders.ts
+++ b/cli/src/utils/resource_folders.ts
@@ -8,7 +8,7 @@
  * (.flow, .app, .raw_app) or dunder-prefixed names (__flow, __app, __raw_app).
  */
 
-import { SEP } from "../../deps.ts";
+import { log, SEP } from "../../deps.ts";
 
 // Resource types that use folder-based storage
 export type FolderResourceType = "flow" | "app" | "raw_app";
@@ -28,7 +28,9 @@ const NON_DOTTED_SUFFIXES = {
   raw_app: "__raw_app",
 } as const;
 
-export type FolderSuffixes = typeof DOTTED_SUFFIXES | typeof NON_DOTTED_SUFFIXES;
+export type FolderSuffixes =
+  | typeof DOTTED_SUFFIXES
+  | typeof NON_DOTTED_SUFFIXES;
 
 // Global state for nonDottedPaths configuration
 let _nonDottedPaths = false;
@@ -39,6 +41,9 @@ let _nonDottedPaths = false;
  * This should be called once at startup based on wmill.yaml configuration.
  */
 export function setNonDottedPaths(value: boolean): void {
+  if (value) {
+    log.info("Using non-dotted paths (__flow, __app, __raw_app)");
+  }
   _nonDottedPaths = value;
 }
 
@@ -148,7 +153,7 @@ export function isRawAppBackendPath(filePath: string): boolean {
   // Normalize path separators for consistent matching
   const normalizedPath = filePath.replaceAll(SEP, "/");
   // Check if path contains pattern: *.[suffix]/backend/
-  const escapedSuffix = suffixes.raw_app.replace(/[.*+?^${}()|[\]\\]/g, '\\$&');
+  const escapedSuffix = suffixes.raw_app.replace(/[.*+?^${}()|[\]\\]/g, "\\$&");
   const pattern = new RegExp(`${escapedSuffix}/backend/`);
   return pattern.test(normalizedPath);
 }
@@ -205,7 +210,12 @@ export function buildMetadataPath(
   type: FolderResourceType,
   format: "yaml" | "json"
 ): string {
-  return resourceName + getFolderSuffixes()[type] + SEP + METADATA_FILES[type][format];
+  return (
+    resourceName +
+    getFolderSuffixes()[type] +
+    SEP +
+    METADATA_FILES[type][format]
+  );
 }
 
 // ============================================================================
@@ -258,27 +268,71 @@ export function extractNameFromFolder(
 // ============================================================================
 
 /**
- * Check if a path ends with a flow metadata file suffix
+ * Check if a path ends with a flow metadata file suffix.
+ * Detects BOTH API format (always dotted: .flow.json) and local format (user-configured).
+ * This is necessary because the API always returns dotted format, but local files
+ * may use non-dotted format if nonDottedPaths is configured.
  */
 export function isFlowMetadataFile(p: string): boolean {
-  const suffixes = getFolderSuffixes();
-  return p.endsWith(suffixes.flow + ".json") || p.endsWith(suffixes.flow + ".yaml");
+  // Always check API format (dotted)
+  if (
+    p.endsWith(DOTTED_SUFFIXES.flow + ".json") ||
+    p.endsWith(DOTTED_SUFFIXES.flow + ".yaml")
+  ) {
+    return true;
+  }
+  // Also check non-dotted format for local files
+  if (_nonDottedPaths) {
+    return (
+      p.endsWith(NON_DOTTED_SUFFIXES.flow + ".json") ||
+      p.endsWith(NON_DOTTED_SUFFIXES.flow + ".yaml")
+    );
+  }
+  return false;
 }
 
 /**
- * Check if a path ends with an app metadata file suffix
+ * Check if a path ends with an app metadata file suffix.
+ * Detects BOTH API format (always dotted: .app.json) and local format (user-configured).
  */
 export function isAppMetadataFile(p: string): boolean {
-  const suffixes = getFolderSuffixes();
-  return p.endsWith(suffixes.app + ".json") || p.endsWith(suffixes.app + ".yaml");
+  // Always check API format (dotted)
+  if (
+    p.endsWith(DOTTED_SUFFIXES.app + ".json") ||
+    p.endsWith(DOTTED_SUFFIXES.app + ".yaml")
+  ) {
+    return true;
+  }
+  // Also check non-dotted format for local files
+  if (_nonDottedPaths) {
+    return (
+      p.endsWith(NON_DOTTED_SUFFIXES.app + ".json") ||
+      p.endsWith(NON_DOTTED_SUFFIXES.app + ".yaml")
+    );
+  }
+  return false;
 }
 
 /**
- * Check if a path ends with a raw_app metadata file suffix
+ * Check if a path ends with a raw_app metadata file suffix.
+ * Detects BOTH API format (always dotted: .raw_app.json) and local format (user-configured).
  */
 export function isRawAppMetadataFile(p: string): boolean {
-  const suffixes = getFolderSuffixes();
-  return p.endsWith(suffixes.raw_app + ".json") || p.endsWith(suffixes.raw_app + ".yaml");
+  // Always check API format (dotted)
+  if (
+    p.endsWith(DOTTED_SUFFIXES.raw_app + ".json") ||
+    p.endsWith(DOTTED_SUFFIXES.raw_app + ".yaml")
+  ) {
+    return true;
+  }
+  // Also check non-dotted format for local files
+  if (_nonDottedPaths) {
+    return (
+      p.endsWith(NON_DOTTED_SUFFIXES.raw_app + ".json") ||
+      p.endsWith(NON_DOTTED_SUFFIXES.raw_app + ".yaml")
+    );
+  }
+  return false;
 }
 
 /**
@@ -308,16 +362,26 @@ export function getDeleteSuffix(
 }
 
 /**
- * Transform a JSON path to the appropriate directory/file path for sync
- * e.g., "f/my_flow.flow.json" -> "f/my_flow.flow" or "f/my_flow__flow.json" -> "f/my_flow__flow"
+ * Transform a JSON path from API format to local directory path for sync.
+ * The API always returns dotted format (.flow.json, .app.json, .raw_app.json).
+ * This function transforms to the user's configured format (dotted or non-dotted).
+ * e.g., with nonDottedPaths=true: "f/my_flow.flow.json" -> "f/my_flow__flow"
+ * e.g., with nonDottedPaths=false: "f/my_flow.flow.json" -> "f/my_flow.flow"
  */
 export function transformJsonPathToDir(
   p: string,
   type: FolderResourceType
 ): string {
-  const suffixes = getFolderSuffixes();
-  const fullSuffix = suffixes[type] + ".json";
-  if (p.endsWith(fullSuffix)) {
+  // API always returns dotted format
+  const apiSuffix = DOTTED_SUFFIXES[type] + ".json";
+  if (p.endsWith(apiSuffix)) {
+    // Remove the API suffix and add user's configured suffix
+    const basePath = p.substring(0, p.length - apiSuffix.length);
+    return basePath + getFolderSuffixes()[type];
+  }
+  // Also handle the case where path already has user's configured format
+  const userSuffix = getFolderSuffixes()[type] + ".json";
+  if (p.endsWith(userSuffix)) {
     return p.substring(0, p.length - 5); // Remove ".json"
   }
   // Path doesn't match expected suffix pattern, return unchanged
diff --git a/cli/src/utils/utils.ts b/cli/src/utils/utils.ts
index 0059fd50c2..b4fa85ba64 100644
--- a/cli/src/utils/utils.ts
+++ b/cli/src/utils/utils.ts
@@ -2,7 +2,7 @@
 // eslint-disable-next-line @typescript-eslint/ban-ts-comment
 // @ts-nocheck This file is copied from a JS project, so it's not type-safe.
 
-import { colors, encodeHex, log } from "../../deps.ts";
+import { colors, encodeHex, log, SEP } from "../../deps.ts";
 import crypto from "node:crypto";
 import { fetchVersion } from "../core/context.ts";
 import { updateGlobalVersions } from "../commands/sync/global.ts";
diff --git a/cli/test/sync_pull_push.test.ts b/cli/test/sync_pull_push.test.ts
index 2443f33e6d..e8409db8c7 100644
--- a/cli/test/sync_pull_push.test.ts
+++ b/cli/test/sync_pull_push.test.ts
@@ -22,6 +22,10 @@ import {
   hasFolderSuffix,
   setNonDottedPaths,
   getNonDottedPaths,
+  isFlowMetadataFile,
+  isAppMetadataFile,
+  isRawAppMetadataFile,
+  transformJsonPathToDir,
 } from "../src/utils/resource_folders.ts";
 
 // =============================================================================
@@ -481,6 +485,123 @@ Deno.test("buildFolderPath creates correct paths", () => {
   assertEquals(buildFolderPath("u/admin/raw_app", "raw_app"), "u/admin/raw_app.raw_app");
 });
 
+// =============================================================================
+// nonDottedPaths Tests - API format detection and transformation
+// =============================================================================
+
+Deno.test("Metadata file detection works with dotted format (default)", () => {
+  // Ensure we're in default mode
+  setNonDottedPaths(false);
+
+  // API always returns dotted format
+  assert(isFlowMetadataFile("f/my_flow.flow.json"), "Should detect .flow.json");
+  assert(isFlowMetadataFile("f/my_flow.flow.yaml"), "Should detect .flow.yaml");
+  assert(isAppMetadataFile("f/my_app.app.json"), "Should detect .app.json");
+  assert(isAppMetadataFile("f/my_app.app.yaml"), "Should detect .app.yaml");
+  assert(isRawAppMetadataFile("f/my_raw.raw_app.json"), "Should detect .raw_app.json");
+  assert(isRawAppMetadataFile("f/my_raw.raw_app.yaml"), "Should detect .raw_app.yaml");
+
+  // Non-matching should return false
+  assert(!isFlowMetadataFile("f/my_script.ts"), "Should not detect script file");
+  assert(!isAppMetadataFile("f/my_script.ts"), "Should not detect script file");
+});
+
+Deno.test("Metadata file detection works with nonDottedPaths=true", () => {
+  // Store original value
+  const wasNonDotted = getNonDottedPaths();
+
+  try {
+    setNonDottedPaths(true);
+
+    // API format (dotted) should still be detected
+    assert(isFlowMetadataFile("f/my_flow.flow.json"), "Should detect API format .flow.json");
+    assert(isAppMetadataFile("f/my_app.app.json"), "Should detect API format .app.json");
+    assert(isRawAppMetadataFile("f/my_raw.raw_app.json"), "Should detect API format .raw_app.json");
+
+    // Local format (non-dotted) should also be detected
+    assert(isFlowMetadataFile("f/my_flow__flow.json"), "Should detect local format __flow.json");
+    assert(isFlowMetadataFile("f/my_flow__flow.yaml"), "Should detect local format __flow.yaml");
+    assert(isAppMetadataFile("f/my_app__app.json"), "Should detect local format __app.json");
+    assert(isRawAppMetadataFile("f/my_raw__raw_app.json"), "Should detect local format __raw_app.json");
+  } finally {
+    // Restore original value
+    setNonDottedPaths(wasNonDotted);
+  }
+});
+
+Deno.test("transformJsonPathToDir transforms API format to local format", () => {
+  // Store original value
+  const wasNonDotted = getNonDottedPaths();
+
+  try {
+    // Test with dotted paths (default)
+    setNonDottedPaths(false);
+    assertEquals(
+      transformJsonPathToDir("f/my_flow.flow.json", "flow"),
+      "f/my_flow.flow",
+      "Should transform dotted API format to dotted local format"
+    );
+    assertEquals(
+      transformJsonPathToDir("f/my_app.app.json", "app"),
+      "f/my_app.app",
+      "Should transform app correctly"
+    );
+    assertEquals(
+      transformJsonPathToDir("f/my_raw.raw_app.json", "raw_app"),
+      "f/my_raw.raw_app",
+      "Should transform raw_app correctly"
+    );
+
+    // Test with non-dotted paths
+    setNonDottedPaths(true);
+    assertEquals(
+      transformJsonPathToDir("f/my_flow.flow.json", "flow"),
+      "f/my_flow__flow",
+      "Should transform dotted API format to non-dotted local format"
+    );
+    assertEquals(
+      transformJsonPathToDir("f/my_app.app.json", "app"),
+      "f/my_app__app",
+      "Should transform app to non-dotted format"
+    );
+    assertEquals(
+      transformJsonPathToDir("f/my_raw.raw_app.json", "raw_app"),
+      "f/my_raw__raw_app",
+      "Should transform raw_app to non-dotted format"
+    );
+
+    // Non-matching paths should be returned unchanged
+    assertEquals(
+      transformJsonPathToDir("f/my_script.ts", "flow"),
+      "f/my_script.ts",
+      "Should return non-matching path unchanged"
+    );
+  } finally {
+    // Restore original value
+    setNonDottedPaths(wasNonDotted);
+  }
+});
+
+Deno.test("getFolderSuffix returns correct suffix based on nonDottedPaths setting", () => {
+  // Store original value
+  const wasNonDotted = getNonDottedPaths();
+
+  try {
+    setNonDottedPaths(false);
+    assertEquals(getFolderSuffix("flow"), ".flow");
+    assertEquals(getFolderSuffix("app"), ".app");
+    assertEquals(getFolderSuffix("raw_app"), ".raw_app");
+
+    setNonDottedPaths(true);
+    assertEquals(getFolderSuffix("flow"), "__flow");
+    assertEquals(getFolderSuffix("app"), "__app");
+    assertEquals(getFolderSuffix("raw_app"), "__raw_app");
+  } finally {
+    // Restore original value
+    setNonDottedPaths(wasNonDotted);
+  }
+});
+
 Deno.test("Script fixture creates valid structure", () => {
   const pythonScript = createScriptFixture("test_script", "python3");