diff --git a/packages/main/src/plugin/directories-legacy.spec.ts b/packages/main/src/plugin/directories-legacy.spec.ts
index 6699725a363..6ec006d8183 100644
--- a/packages/main/src/plugin/directories-legacy.spec.ts
+++ b/packages/main/src/plugin/directories-legacy.spec.ts
@@ -177,6 +177,18 @@ describe('LegacyDirectories', () => {
       expect(provider.getManagedDefaultsDirectory()).toBe(product.paths.managed.linux);
     });
 
+    test('should return flatpak managed folder path when running on Linux in Flatpak', () => {
+      vi.mocked(isMac).mockReturnValue(false);
+      vi.mocked(isWindows).mockReturnValue(false);
+      vi.mocked(isLinux).mockReturnValue(true);
+      // biome-ignore lint/complexity/useLiteralKeys: FLATPAK_ID comes from an index signature
+      process.env['FLATPAK_ID'] = 'io.podman_desktop.PodmanDesktop';
+
+      provider = new LegacyDirectories();
+
+      expect(provider.getManagedDefaultsDirectory()).toBe(product.paths.managed.flatpak);
+    });
+
     test('should fallback to linux managed folder path when platform is unknown', () => {
       vi.mocked(isMac).mockReturnValue(false);
       vi.mocked(isWindows).mockReturnValue(false);
diff --git a/packages/main/src/plugin/directories-legacy.ts b/packages/main/src/plugin/directories-legacy.ts
index 51c27eebd88..5d7d1f8c4bd 100644
--- a/packages/main/src/plugin/directories-legacy.ts
+++ b/packages/main/src/plugin/directories-legacy.ts
@@ -103,6 +103,10 @@ export class LegacyDirectories implements Directories {
       // replace %PROGRAMDATA% in the path
       return product.paths.managed.windows.replace('%PROGRAMDATA%', programData);
     } else if (isLinux()) {
+      // biome-ignore lint/complexity/useLiteralKeys: FLATPAK_ID comes from an index signature
+      if (process.env['FLATPAK_ID']) {
+        return product.paths.managed.flatpak;
+      }
       return product.paths.managed.linux;
     }
     // Fallback to Linux-style path
diff --git a/packages/main/src/plugin/directories-linux-xdg.spec.ts b/packages/main/src/plugin/directories-linux-xdg.spec.ts
index af98e298c91..25510a3e622 100644
--- a/packages/main/src/plugin/directories-linux-xdg.spec.ts
+++ b/packages/main/src/plugin/directories-linux-xdg.spec.ts
@@ -21,6 +21,8 @@ import * as path from 'node:path';
 
 import { afterEach, beforeEach, describe, expect, test, vi } from 'vitest';
 
+import product from '/@product.json' with { type: 'json' };
+
 import type { Directories } from './directories.js';
 import { LinuxXDGDirectories } from './directories-linux-xdg.js';
 
@@ -35,6 +37,8 @@ beforeEach(() => {
   delete process.env['XDG_CONFIG_HOME'];
   // biome-ignore lint/complexity/useLiteralKeys: XDG_DATA_HOME comes from an index signature
   delete process.env['XDG_DATA_HOME'];
+  // biome-ignore lint/complexity/useLiteralKeys: FLATPAK_ID comes from an index signature
+  delete process.env['FLATPAK_ID'];
 });
 
 afterEach(() => {
@@ -115,4 +119,21 @@ describe('LinuxXDGDirectories', () => {
       expect(provider.getExtensionsStorageDirectory()).toBe(path.resolve(expectedDataDir, 'extensions-storage'));
     });
   });
+
+  describe('getManagedDefaultsDirectory', () => {
+    test('should return linux managed folder path when not running in Flatpak', () => {
+      provider = new LinuxXDGDirectories();
+
+      expect(provider.getManagedDefaultsDirectory()).toBe(product.paths.managed.linux);
+    });
+
+    test('should return flatpak managed folder path when running in Flatpak', () => {
+      // biome-ignore lint/complexity/useLiteralKeys: FLATPAK_ID comes from an index signature
+      process.env['FLATPAK_ID'] = 'io.podman_desktop.PodmanDesktop';
+
+      provider = new LinuxXDGDirectories();
+
+      expect(provider.getManagedDefaultsDirectory()).toBe(product.paths.managed.flatpak);
+    });
+  });
 });
diff --git a/packages/main/src/plugin/directories-linux-xdg.ts b/packages/main/src/plugin/directories-linux-xdg.ts
index 40b049b77ff..ed16715a00d 100644
--- a/packages/main/src/plugin/directories-linux-xdg.ts
+++ b/packages/main/src/plugin/directories-linux-xdg.ts
@@ -87,6 +87,10 @@ export class LinuxXDGDirectories implements Directories {
   }
 
   getManagedDefaultsDirectory(): string {
+    // biome-ignore lint/complexity/useLiteralKeys: FLATPAK_ID comes from an index signature
+    if (process.env['FLATPAK_ID']) {
+      return product.paths.managed.flatpak;
+    }
     return product.paths.managed.linux;
   }
 }
diff --git a/product.json b/product.json
index 62c62936c47..4a050f05220 100644
--- a/product.json
+++ b/product.json
@@ -9,7 +9,8 @@
     "managed": {
       "macOS": "/Library/Application Support/io.podman_desktop.PodmanDesktop",
       "windows": "%PROGRAMDATA%\\Podman Desktop",
-      "linux": "/usr/share/podman-desktop"
+      "linux": "/usr/share/podman-desktop",
+      "flatpak": "/run/host/usr/share/podman-desktop"
     }
   },
   "telemetry": {