diff --git a/public/openapi/components/schemas/CategoryObject.yaml b/public/openapi/components/schemas/CategoryObject.yaml
index 4d6cb0ca4e..0b138542b0 100644
--- a/public/openapi/components/schemas/CategoryObject.yaml
+++ b/public/openapi/components/schemas/CategoryObject.yaml
@@ -8,6 +8,14 @@ CategoryObject:
         name:
           type: string
           description: The category's name/title
+        handle:
+          type: string
+          description: |
+            An URL-safe name/handle used to represent the category over federated networks (e.g. ActivityPub).
+
+            This value is separate from the `slug`, which is used specifically in the URL as a human-readable representation.
+
+            The handle is unique across-the-board between users/groups/categories.
         description:
           type: string
           description: A variable-length description of the category (usually displayed underneath the category name)
diff --git a/src/categories/create.js b/src/categories/create.js
index 92924eb6dd..745c8b9d73 100644
--- a/src/categories/create.js
+++ b/src/categories/create.js
@@ -5,6 +5,7 @@ const _ = require('lodash');
 
 const db = require('../database');
 const plugins = require('../plugins');
+const meta = require('../meta');
 const privileges = require('../privileges');
 const utils = require('../utils');
 const slugify = require('../slugify');
@@ -20,6 +21,7 @@ module.exports = function (Categories) {
 
 		data.name = String(data.name || `Category ${cid}`);
 		const slug = `${cid}/${slugify(data.name)}`;
+		const handle = await Categories.generateHandle(slugify(data.name));
 		const smallestOrder = firstChild.length ? firstChild[0].score - 1 : 1;
 		const order = data.order || smallestOrder; // If no order provided, place it at the top
 		const colours = Categories.assignColours();
@@ -27,6 +29,7 @@ module.exports = function (Categories) {
 		let category = {
 			cid: cid,
 			name: data.name,
+			handle,
 			description: data.description ? data.description : '',
 			descriptionParsed: data.descriptionParsed ? data.descriptionParsed : '',
 			icon: data.icon ? data.icon : '',
@@ -146,6 +149,19 @@ module.exports = function (Categories) {
 		await async.each(children, Categories.create);
 	}
 
+	async function generateHandle(slug) {
+		let taken = await meta.slugTaken(slug);
+		let suffix;
+		while (taken) {
+			suffix = utils.generateUUID().slice(0, 8);
+			// eslint-disable-next-line no-await-in-loop
+			taken = await meta.slugTaken(`${slug}-${suffix}`);
+		}
+
+		return `${slug}${suffix ? `-${suffix}` : ''}`;
+	}
+	Categories.generateHandle = generateHandle; // exported for upgrade script (4.0.0)
+
 	Categories.assignColours = function () {
 		const backgrounds = ['#AB4642', '#DC9656', '#F7CA88', '#A1B56C', '#86C1B9', '#7CAFC2', '#BA8BAF', '#A16946'];
 		const text = ['#ffffff', '#ffffff', '#333333', '#ffffff', '#333333', '#ffffff', '#ffffff', '#ffffff'];
diff --git a/src/categories/index.js b/src/categories/index.js
index 54346d5a64..bbdf9f7ece 100644
--- a/src/categories/index.js
+++ b/src/categories/index.js
@@ -30,6 +30,13 @@ Categories.exists = async function (cids) {
 	);
 };
 
+Categories.existsByHandle = async function (handle) {
+	if (Array.isArray(handle)) {
+		return await db.isSortedSetMembers('categoryhandle:cid', handle);
+	}
+	return await db.isSortedSetMember('categoryhandle:cid', handle);
+};
+
 Categories.getCategoryById = async function (data) {
 	const categories = await Categories.getCategories([data.cid]);
 	if (!categories[0]) {
@@ -67,6 +74,10 @@ Categories.getCategoryById = async function (data) {
 	return result.category;
 };
 
+Categories.getCidByHandle = async function (handle) {
+	return await db.sortedSetScore('categoryhandle:cid', handle);
+};
+
 Categories.getAllCidsFromSet = async function (key) {
 	let cids = cache.get(key);
 	if (cids) {
diff --git a/src/controllers/well-known.js b/src/controllers/well-known.js
index 2cc91da6a6..93a0839176 100644
--- a/src/controllers/well-known.js
+++ b/src/controllers/well-known.js
@@ -19,18 +19,21 @@ Controller.webfinger = async (req, res) => {
 
 	// Get the slug
 	const slug = resource.slice(5, resource.length - (host.length + 1));
-	const uid = await user.getUidByUserslug(slug);
+	const [uid, cid] = await Promise.all([
+		user.getUidByUserslug(slug),
+		categories.getCidByHandle(slug),
+	]);
 	let response = {
 		subject: `acct:${slug}@${host}`,
 	};
 
 	try {
-		if (slug.startsWith('cid.')) {
-			response = await category(req.uid, slug.slice(4), response);
-		} else if (slug === hostname) {
+		if (slug === hostname) {
 			response = application(response);
 		} else if (uid) {
 			response = await profile(req.uid, uid, response);
+		} else if (cid) {
+			response = await category(req.uid, cid, response);
 		} else {
 			return res.sendStatus(404);
 		}
diff --git a/src/groups/create.js b/src/groups/create.js
index 74ef56a41f..3b8b5da669 100644
--- a/src/groups/create.js
+++ b/src/groups/create.js
@@ -18,7 +18,7 @@ module.exports = function (Groups) {
 
 		Groups.validateGroupName(data.name);
 
-		const exists = await meta.userOrGroupExists(data.name);
+		const exists = await meta.slugTaken(data.name);
 		if (exists) {
 			throw new Error('[[error:group-already-exists]]');
 		}
diff --git a/src/meta/index.js b/src/meta/index.js
index 487c53df60..464ce3dea8 100644
--- a/src/meta/index.js
+++ b/src/meta/index.js
@@ -25,19 +25,20 @@ Meta.blacklist = require('./blacklist');
 Meta.languages = require('./languages');
 
 
-/* Assorted */
-Meta.userOrGroupExists = async function (slug) {
+Meta.slugTaken = async function (slug) {
 	if (!slug) {
 		throw new Error('[[error:invalid-data]]');
 	}
-	const user = require('../user');
-	const groups = require('../groups');
+
+	const [user, groups, categories] = [require('../user'), require('../groups'), require('../categories')];
 	slug = slugify(slug);
-	const [userExists, groupExists] = await Promise.all([
+
+	const exists = await Promise.all([
 		user.existsBySlug(slug),
 		groups.existsBySlug(slug),
+		categories.existsByHandle(slug),
 	]);
-	return userExists || groupExists;
+	return exists.some(Boolean);
 };
 
 if (nconf.get('isPrimary')) {
diff --git a/src/upgrades/4.0.0/activitypub_setup.js b/src/upgrades/4.0.0/activitypub_setup.js
index 6e30020b8a..fdc93f2fdf 100644
--- a/src/upgrades/4.0.0/activitypub_setup.js
+++ b/src/upgrades/4.0.0/activitypub_setup.js
@@ -1,7 +1,9 @@
 'use strict';
 
-// const db = require('../../database');
+const db = require('../../database');
 const meta = require('../../meta');
+const categories = require('../../categories');
+const slugify = require('../../slugify');
 
 module.exports = {
 	name: 'Setting up default configs/privileges re: ActivityPub',
@@ -13,5 +15,20 @@ module.exports = {
 		// Set default privileges for world category
 		const install = require('../../install');
 		await install.giveWorldPrivileges();
+
+		// Run through all categories and ensure their slugs are unique (incl. users/groups too)
+		const cids = await db.getSortedSetMembers('categories:cid');
+		const names = await db.getObjectsFields(cids.map(cid => `category:${cid}`), cids.map(() => 'name'));
+
+		const handles = await Promise.all(cids.map(async (cid, idx) => {
+			const { name } = names[idx];
+			const handle = await categories.generateHandle(slugify(name));
+			return handle;
+		}));
+
+		await Promise.all([
+			db.setObjectBulk(cids.map((cid, idx) => [`category:${cid}`, { handle: handles[idx] }])),
+			db.sortedSetAdd('categoryhandle:cid', cids, handles),
+		]);
 	},
 };
diff --git a/src/user/create.js b/src/user/create.js
index 610d614e81..7cdfb3c4cf 100644
--- a/src/user/create.js
+++ b/src/user/create.js
@@ -184,7 +184,7 @@ module.exports = function (User) {
 		let { username } = userData;
 		while (true) {
 			/* eslint-disable no-await-in-loop */
-			const exists = await meta.userOrGroupExists(username);
+			const exists = await meta.slugTaken(username);
 			if (!exists) {
 				return numTries ? username : null;
 			}