diff --git a/packages/core/integration-tests/test/integration/webmanifest-json/file-handler-icon.png b/packages/core/integration-tests/test/integration/webmanifest-json/file-handler-icon.png
new file mode 100644
index 00000000000..8a1daa0121d
Binary files /dev/null and b/packages/core/integration-tests/test/integration/webmanifest-json/file-handler-icon.png differ
diff --git a/packages/core/integration-tests/test/integration/webmanifest-json/manifest.json b/packages/core/integration-tests/test/integration/webmanifest-json/manifest.json
index bf9b21d989b..6111282a874 100644
--- a/packages/core/integration-tests/test/integration/webmanifest-json/manifest.json
+++ b/packages/core/integration-tests/test/integration/webmanifest-json/manifest.json
@@ -16,14 +16,26 @@
   ],
   "shortcuts": [
     {
-        "name": "example-shortcut",
-        "icons": [
-            {
-                "src": "shortcut-icon.png",
-                "sizes": "100x100",
-                "type": "image/png"
-            }
-        ]
+      "name": "example-shortcut",
+      "icons": [
+        {
+          "src": "shortcut-icon.png",
+          "sizes": "100x100",
+          "type": "image/png"
+        }
+      ]
+    }
+  ],
+  "file_handlers": [
+    {
+      "name": "example-file-handler",
+      "icons": [
+        {
+          "src": "file-handler-icon.png",
+          "sizes": "100x100",
+          "type": "image/png"
+        }
+      ]
     }
   ]
 }
diff --git a/packages/core/integration-tests/test/integration/webmanifest-schema/manifest.webmanifest b/packages/core/integration-tests/test/integration/webmanifest-schema/manifest.webmanifest
index 7b9bf17e5db..60168aaeada 100644
--- a/packages/core/integration-tests/test/integration/webmanifest-schema/manifest.webmanifest
+++ b/packages/core/integration-tests/test/integration/webmanifest-schema/manifest.webmanifest
@@ -31,5 +31,6 @@
         {}
       ]
     }
-  ]
+  ],
+  "file_handlers": {}
 }
diff --git a/packages/core/integration-tests/test/integration/webmanifest/file-handler-icon.png b/packages/core/integration-tests/test/integration/webmanifest/file-handler-icon.png
new file mode 100644
index 00000000000..8a1daa0121d
Binary files /dev/null and b/packages/core/integration-tests/test/integration/webmanifest/file-handler-icon.png differ
diff --git a/packages/core/integration-tests/test/integration/webmanifest/manifest.webmanifest b/packages/core/integration-tests/test/integration/webmanifest/manifest.webmanifest
index bf9b21d989b..6111282a874 100644
--- a/packages/core/integration-tests/test/integration/webmanifest/manifest.webmanifest
+++ b/packages/core/integration-tests/test/integration/webmanifest/manifest.webmanifest
@@ -16,14 +16,26 @@
   ],
   "shortcuts": [
     {
-        "name": "example-shortcut",
-        "icons": [
-            {
-                "src": "shortcut-icon.png",
-                "sizes": "100x100",
-                "type": "image/png"
-            }
-        ]
+      "name": "example-shortcut",
+      "icons": [
+        {
+          "src": "shortcut-icon.png",
+          "sizes": "100x100",
+          "type": "image/png"
+        }
+      ]
+    }
+  ],
+  "file_handlers": [
+    {
+      "name": "example-file-handler",
+      "icons": [
+        {
+          "src": "file-handler-icon.png",
+          "sizes": "100x100",
+          "type": "image/png"
+        }
+      ]
     }
   ]
 }
diff --git a/packages/core/integration-tests/test/webmanifest.js b/packages/core/integration-tests/test/webmanifest.js
index 7b0ce812d4e..9c6cc091297 100644
--- a/packages/core/integration-tests/test/webmanifest.js
+++ b/packages/core/integration-tests/test/webmanifest.js
@@ -30,6 +30,10 @@ describe('webmanifest', function () {
         type: 'png',
         assets: ['shortcut-icon.png'],
       },
+      {
+        type: 'png',
+        assets: ['file-handler-icon.png'],
+      },
     ]);
 
     const manifest = await outputFS.readFile(
@@ -39,6 +43,7 @@ describe('webmanifest', function () {
     assert(/screenshot\.[0-9a-f]+\.png/.test(manifest));
     assert(/icon\.[0-9a-f]+\.png/.test(manifest));
     assert(/shortcut-icon\.[0-9a-f]+\.png/.test(manifest));
+    assert(/file-handler-icon\.[0-9a-f]+\.png/.test(manifest));
   });
 
   it('should support .json', async function () {
@@ -67,6 +72,10 @@ describe('webmanifest', function () {
         type: 'png',
         assets: ['shortcut-icon.png'],
       },
+      {
+        type: 'png',
+        assets: ['file-handler-icon.png'],
+      },
     ]);
 
     const manifest = await outputFS.readFile(
@@ -76,9 +85,10 @@ describe('webmanifest', function () {
     assert(/screenshot\.[0-9a-f]+\.png/.test(manifest));
     assert(/icon\.[0-9a-f]+\.png/.test(manifest));
     assert(/shortcut-icon\.[0-9a-f]+\.png/.test(manifest));
+    assert(/file-handler-icon\.[0-9a-f]+\.png/.test(manifest));
   });
 
-  it('should throw on malformed icons and screenshots', async function () {
+  it('should throw on malformed icons, screenshots, shortcuts, and file handlers', async function () {
     let manifestPath = path.join(
       __dirname,
       '/integration/webmanifest-schema/manifest.webmanifest',
@@ -167,6 +177,17 @@ describe('webmanifest', function () {
                       line: 31,
                     },
                   },
+                  {
+                    end: {
+                      column: 21,
+                      line: 35,
+                    },
+                    message: 'Expected type array',
+                    start: {
+                      column: 20,
+                      line: 35,
+                    },
+                  },
                 ],
               },
             ],
diff --git a/packages/transformers/webmanifest/src/WebManifestTransformer.js b/packages/transformers/webmanifest/src/WebManifestTransformer.js
index 3288a9c330a..a6307df5efc 100644
--- a/packages/transformers/webmanifest/src/WebManifestTransformer.js
+++ b/packages/transformers/webmanifest/src/WebManifestTransformer.js
@@ -39,6 +39,15 @@ const MANIFEST_SCHEMA: SchemaEntity = {
         },
       },
     },
+    file_handlers: {
+      type: 'array',
+      items: {
+        type: 'object',
+        properties: {
+          icons: RESOURCES_SCHEMA,
+        },
+      },
+    },
   },
 };
 
@@ -54,8 +63,7 @@ export default (new Transformer({
       'Invalid webmanifest',
     );
 
-    for (const key of ['icons', 'screenshots']) {
-      const list = data[key];
+    function addResourceListToAsset(list, parent) {
       if (list) {
         invariant(Array.isArray(list));
         for (let i = 0; i < list.length; i++) {
@@ -63,31 +71,28 @@ export default (new Transformer({
           res.src = asset.addURLDependency(res.src, {
             loc: {
               filePath: asset.filePath,
-              ...getJSONSourceLocation(pointers[`/${key}/${i}/src`], 'value'),
+              ...getJSONSourceLocation(
+                pointers[`/${parent}/${i}/src`],
+                'value',
+              ),
             },
           });
         }
       }
     }
 
-    if (data.shortcuts) {
-      invariant(Array.isArray(data.shortcuts));
-      for (let i = 0; i < data.shortcuts.length; i++) {
-        const list = data.shortcuts[i].icons;
-        if (list) {
-          invariant(Array.isArray(list));
-          for (let j = 0; j < list.length; j++) {
-            const res = list[j];
-            res.src = asset.addURLDependency(res.src, {
-              loc: {
-                filePath: asset.filePath,
-                ...getJSONSourceLocation(
-                  pointers[`/shortcuts/${i}/icons/${j}/src`],
-                  'value',
-                ),
-              },
-            });
-          }
+    for (const key of ['icons', 'screenshots']) {
+      const list = data[key];
+      addResourceListToAsset(list, key);
+    }
+
+    for (const key of ['shortcuts', 'file_handlers']) {
+      const list = data[key];
+      if (list) {
+        invariant(Array.isArray(list));
+        for (let i = 0; i < list.length; i++) {
+          const iconList = list[i].icons;
+          addResourceListToAsset(iconList, `${key}/${i}/icons`);
         }
       }
     }