diff --git a/src/parsers/manifestjson.js b/src/parsers/manifestjson.js
index 60e85909fbf..3e33be245bf 100644
--- a/src/parsers/manifestjson.js
+++ b/src/parsers/manifestjson.js
@@ -52,6 +52,13 @@ async function getImageMetadata(io, iconPath) {
   return probeImageSize(data);
 }
 
+function getNormalizedExtension(_path) {
+  return path
+    .extname(_path)
+    .substring(1)
+    .toLowerCase();
+}
+
 export default class ManifestJSONParser extends JSONParser {
   constructor(
     jsonString,
@@ -499,22 +506,58 @@ export default class ManifestJSONParser extends JSONParser {
   }
 
   validateIcons() {
+    const icons = [];
+
+    if (this.parsedJSON.icons) {
+      Object.keys(this.parsedJSON.icons).forEach((size) => {
+        icons.push([size, this.parsedJSON.icons[size]]);
+      });
+    }
+
+    // Check for default_icon key at each of the action properties
+    ['browser_action', 'page_action', 'sidebar_action'].forEach((key) => {
+      if (this.parsedJSON[key] && this.parsedJSON[key].default_icon) {
+        if (typeof this.parsedJSON[key].default_icon === 'string') {
+          icons.push([null, this.parsedJSON[key].default_icon]);
+        } else {
+          Object.keys(this.parsedJSON[key].default_icon).forEach((size) => {
+            icons.push([size, this.parsedJSON[key].default_icon[size]]);
+          });
+        }
+      }
+    });
+
+    // Check for the theme_icons from the browser_action
+    if (
+      this.parsedJSON.browser_action &&
+      this.parsedJSON.browser_action.theme_icons
+    ) {
+      this.parsedJSON.browser_action.theme_icons.forEach((icon) => {
+        if (icon.dark) {
+          icons.push([icon.size, icon.dark]);
+        }
+        if (icon.light) {
+          icons.push([icon.size, icon.light]);
+        }
+      });
+    }
+
     const promises = [];
-    const { icons } = this.parsedJSON;
-    Object.keys(icons).forEach((size) => {
-      const _path = normalizePath(icons[size]);
+    const errorIcons = [];
+    icons.forEach(([size, iconPath]) => {
+      const _path = normalizePath(iconPath);
       if (!Object.prototype.hasOwnProperty.call(this.io.files, _path)) {
-        this.collector.addError(messages.manifestIconMissing(_path));
-        this.isValid = false;
+        if (!errorIcons.includes(_path)) {
+          this.collector.addError(messages.manifestIconMissing(_path));
+          this.isValid = false;
+          errorIcons.push(_path);
+        }
       } else if (
-        !IMAGE_FILE_EXTENSIONS.includes(
-          _path
-            .split('.')
-            .pop()
-            .toLowerCase()
-        )
+        !IMAGE_FILE_EXTENSIONS.includes(getNormalizedExtension(_path))
       ) {
-        this.collector.addWarning(messages.WRONG_ICON_EXTENSION);
+        if (!errorIcons.includes(_path)) {
+          this.collector.addWarning(messages.WRONG_ICON_EXTENSION);
+        }
       } else {
         promises.push(this.validateIcon(_path, size));
       }
@@ -524,10 +567,7 @@ export default class ManifestJSONParser extends JSONParser {
 
   async validateThemeImage(imagePath, manifestPropName) {
     const _path = normalizePath(imagePath);
-    const ext = path
-      .extname(imagePath)
-      .substring(1)
-      .toLowerCase();
+    const ext = getNormalizedExtension(imagePath);
 
     const fileExists = this.validateFileExistsInPackage(
       _path,
diff --git a/tests/unit/helpers.js b/tests/unit/helpers.js
index 2e8e9b244c3..42d88e359b2 100644
--- a/tests/unit/helpers.js
+++ b/tests/unit/helpers.js
@@ -256,6 +256,12 @@ export function assertHasMatchingError(errors, expected) {
   expect(errors.some((error) => isMatch(error, expected))).toBe(true);
 }
 
+export function assertHasMatchingErrorCount(errors, expected, count) {
+  expect(Array.isArray(errors)).toBe(true);
+  expect(errors.length).toBeGreaterThan(0);
+  expect(errors.filter((error) => isMatch(error, expected)).length).toBe(count);
+}
+
 export function getStreamableIO(files) {
   return {
     files,
diff --git a/tests/unit/parsers/test.manifestjson.js b/tests/unit/parsers/test.manifestjson.js
index 4e5c2c860a1..3c71b8f2641 100644
--- a/tests/unit/parsers/test.manifestjson.js
+++ b/tests/unit/parsers/test.manifestjson.js
@@ -9,6 +9,7 @@ import * as messages from 'messages';
 
 import {
   assertHasMatchingError,
+  assertHasMatchingErrorCount,
   validManifestJSON,
   validDictionaryManifestJSON,
   validLangpackManifestJSON,
@@ -1219,6 +1220,164 @@ describe('ManifestJSONParser', () => {
       });
     });
 
+    it('adds an error if the browser_action icon is not in the package', async () => {
+      const addonLinter = new Linter({ _: ['bar'] });
+      const json = validManifestJSON({
+        browser_action: {
+          default_icon: {
+            32: 'icons/icon-32.png',
+            64: 'icons/icon-64.png',
+          },
+        },
+      });
+      const files = {
+        'icons/icon-32.png': EMPTY_PNG.toString('binary'),
+      };
+      const manifestJSONParser = new ManifestJSONParser(
+        json,
+        addonLinter.collector,
+        { io: getStreamableIO(files) }
+      );
+
+      await manifestJSONParser.validateIcons();
+      expect(manifestJSONParser.isValid).toBeFalsy();
+      assertHasMatchingError(addonLinter.collector.errors, {
+        code: messages.MANIFEST_ICON_NOT_FOUND,
+        message:
+          'An icon defined in the manifest could not be found in the package.',
+        description: 'Icon could not be found at "icons/icon-64.png".',
+      });
+    });
+
+    it('adds an error if the browser_action theme icon is not in the package', async () => {
+      const addonLinter = new Linter({ _: ['bar'] });
+      const json = validManifestJSON({
+        browser_action: {
+          theme_icons: [
+            {
+              light: 'icons/light-32.png',
+              dark: 'icons/dark-32.png',
+              size: 32,
+            },
+          ],
+        },
+      });
+      const files = {
+        'icons/light-32.png': EMPTY_PNG.toString('binary'),
+      };
+      const manifestJSONParser = new ManifestJSONParser(
+        json,
+        addonLinter.collector,
+        { io: getStreamableIO(files) }
+      );
+
+      await manifestJSONParser.validateIcons();
+      expect(manifestJSONParser.isValid).toBeFalsy();
+      assertHasMatchingError(addonLinter.collector.errors, {
+        code: messages.MANIFEST_ICON_NOT_FOUND,
+        message:
+          'An icon defined in the manifest could not be found in the package.',
+        description: 'Icon could not be found at "icons/dark-32.png".',
+      });
+    });
+
+    it('adds an error if the page_action icon is not in the package', async () => {
+      const addonLinter = new Linter({ _: ['bar'] });
+      const json = validManifestJSON({
+        page_action: {
+          default_icon: {
+            32: 'icons/icon-32.png',
+            64: 'icons/icon-64.png',
+          },
+        },
+      });
+      const files = {
+        'icons/icon-32.png': EMPTY_PNG.toString('binary'),
+      };
+      const manifestJSONParser = new ManifestJSONParser(
+        json,
+        addonLinter.collector,
+        { io: getStreamableIO(files) }
+      );
+
+      await manifestJSONParser.validateIcons();
+      expect(manifestJSONParser.isValid).toBeFalsy();
+      assertHasMatchingError(addonLinter.collector.errors, {
+        code: messages.MANIFEST_ICON_NOT_FOUND,
+        message:
+          'An icon defined in the manifest could not be found in the package.',
+        description: 'Icon could not be found at "icons/icon-64.png".',
+      });
+    });
+
+    it('adds an error if the sidebar_action icon is not in the package', async () => {
+      const addonLinter = new Linter({ _: ['bar'] });
+      const json = validManifestJSON({
+        sidebar_action: {
+          default_icon: {
+            32: 'icons/icon-32.png',
+            64: 'icons/icon-64.png',
+          },
+        },
+      });
+      const files = {
+        'icons/icon-32.png': EMPTY_PNG.toString('binary'),
+      };
+      const manifestJSONParser = new ManifestJSONParser(
+        json,
+        addonLinter.collector,
+        { io: getStreamableIO(files) }
+      );
+
+      await manifestJSONParser.validateIcons();
+      expect(manifestJSONParser.isValid).toBeFalsy();
+      assertHasMatchingError(addonLinter.collector.errors, {
+        code: messages.MANIFEST_ICON_NOT_FOUND,
+        message:
+          'An icon defined in the manifest could not be found in the package.',
+        description: 'Icon could not be found at "icons/icon-64.png".',
+      });
+    });
+
+    it('filters duplicate errors if a missing icon is reused', async () => {
+      const addonLinter = new Linter({ _: ['bar'] });
+      const json = validManifestJSON({
+        browser_action: {
+          default_icon: {
+            32: 'icons/icon-32.png',
+            64: 'icons/icon-64.png',
+          },
+        },
+        sidebar_action: {
+          default_icon: {
+            32: 'icons/icon-32.png',
+            64: 'icons/icon-64.png',
+          },
+        },
+      });
+      const files = {
+        'icons/icon-32.png': EMPTY_PNG.toString('binary'),
+      };
+      const manifestJSONParser = new ManifestJSONParser(
+        json,
+        addonLinter.collector,
+        { io: getStreamableIO(files) }
+      );
+
+      await manifestJSONParser.validateIcons();
+      expect(manifestJSONParser.isValid).toBeFalsy();
+      assertHasMatchingErrorCount(
+        addonLinter.collector.errors,
+        {
+          code: messages.MANIFEST_ICON_NOT_FOUND,
+          message:
+            'An icon defined in the manifest could not be found in the package.',
+          description: 'Icon could not be found at "icons/icon-64.png".',
+        },
+        1
+      );
+    });
+
     it('adds a warning if the icon does not have a valid extension', async () => {
       const addonLinter = new Linter({ _: ['bar'] });
       const json = validManifestJSON({