diff --git a/ghost/core/core/server/api/endpoints/collections.js b/ghost/core/core/server/api/endpoints/collections.js
index 92e6ffb06b..2bf31facbe 100644
--- a/ghost/core/core/server/api/endpoints/collections.js
+++ b/ghost/core/core/server/api/endpoints/collections.js
@@ -29,7 +29,11 @@ module.exports = {
         },
         permissions: true,
         query(frame) {
-            return collectionsService.api.getAll(frame.options);
+            return collectionsService.api.getAll({
+                filter: frame.options.filter,
+                limit: frame.options.limit,
+                page: frame.options.page
+            });
         }
     },
 
diff --git a/ghost/core/core/server/services/collections/BookshelfCollectionsRepository.js b/ghost/core/core/server/services/collections/BookshelfCollectionsRepository.js
index 3a05bfccf1..855226d756 100644
--- a/ghost/core/core/server/services/collections/BookshelfCollectionsRepository.js
+++ b/ghost/core/core/server/services/collections/BookshelfCollectionsRepository.js
@@ -28,12 +28,14 @@ module.exports = class BookshelfCollectionsRepository {
     async getById(id, options = {}) {
         const model = await this.#model.findOne({id}, {
             require: false,
-            withRelated: ['collectionPosts'],
             transacting: options.transaction
         });
         if (!model) {
             return null;
         }
+
+        model.collectionPostIds = await this.#fetchCollectionPostIds(model.id, options);
+
         return this.#modelToCollection(model);
     }
 
@@ -44,28 +46,63 @@ module.exports = class BookshelfCollectionsRepository {
     async getBySlug(slug, options = {}) {
         const model = await this.#model.findOne({slug}, {
             require: false,
-            withRelated: ['collectionPosts'],
             transacting: options.transaction
         });
+
         if (!model) {
             return null;
         }
+
+        model.collectionPostIds = await this.#fetchCollectionPostIds(model.id, options);
+
         return this.#modelToCollection(model);
     }
 
+    /**
+     * NOTE: we are only fetching post_id column here to save memory on
+     *       instances with a large amount of posts
+     *
+     *       The method could be further optimized to fetch posts for
+     *       multiple collections at a time.
+     *
+     * @param {string} collectionId collection to fetch post ids for
+     * @param {Object} options bookshelf options
+     *
+     * @returns {Promise<Array<{post_id: string}>>}
+     */
+    async #fetchCollectionPostIds(collectionId, options = {}) {
+        const toSelect = options.columns || ['post_id'];
+
+        const query = this.#relationModel.query();
+        if (options.transaction) {
+            query.transacting(options.transaction);
+        }
+
+        return await query
+            .select(toSelect)
+            .where('collection_id', collectionId);
+    }
+
     /**
      * @param {object} [options]
      * @param {string} [options.filter]
      * @param {string} [options.order]
+     * @param {string[]} [options.withRelated]
      * @param {import('knex').Transaction} [options.transaction]
      */
     async getAll(options = {}) {
         const models = await this.#model.findAll({
             ...options,
-            transacting: options.transaction,
-            withRelated: ['collectionPosts']
+            transacting: options.transaction
         });
 
+        for (const model of models) {
+            // NOTE: Ideally collection posts would be fetching as a part of findAll query.
+            //       Because bookshelf introduced a massive processing and memory overhead
+            //       we are fetching collection post ids separately using raw knex query
+            model.collectionPostIds = await this.#fetchCollectionPostIds(model.id, options);
+        }
+
         return (await Promise.all(models.map(model => this.#modelToCollection(model)))).filter(entity => !!entity);
     }
 
@@ -78,6 +115,10 @@ module.exports = class BookshelfCollectionsRepository {
         }
 
         try {
+            // NOTE: collectionPosts are not a part of serialized model
+            //       and are fetched separately to save memory
+            const posts = model.collectionPostIds;
+
             return await Collection.create({
                 id: json.id,
                 slug: json.slug,
@@ -86,7 +127,7 @@ module.exports = class BookshelfCollectionsRepository {
                 filter: filter,
                 type: json.type,
                 featureImage: json.feature_image,
-                posts: json.collectionPosts.map(collectionPost => collectionPost.post_id),
+                posts: posts.map(collectionPost => collectionPost.post_id),
                 createdAt: json.created_at,
                 updatedAt: json.updated_at
             });
@@ -135,8 +176,7 @@ module.exports = class BookshelfCollectionsRepository {
             {id: data.id},
             {
                 require: false,
-                transacting: options.transaction,
-                withRelated: ['collectionPosts']
+                transacting: options.transaction
             }
         );
 
@@ -175,7 +215,11 @@ module.exports = class BookshelfCollectionsRepository {
             if (collection.type === 'manual') {
                 await this.#relationModel.query().delete().where('collection_id', collection.id).transacting(options.transaction);
             } else {
-                const existingRelations = existing.toJSON().collectionPosts;
+                const collectionPostsOptions = {
+                    transaction: options.transaction,
+                    columns: ['id', 'post_id']
+                };
+                const existingRelations = await this.#fetchCollectionPostIds(collection.id, collectionPostsOptions);
 
                 for (const existingRelation of existingRelations) {
                     const found = collectionPostsRelations.find((thing) => {
diff --git a/ghost/core/test/e2e-api/admin/collections.test.js b/ghost/core/test/e2e-api/admin/collections.test.js
index 917832e154..96d362a171 100644
--- a/ghost/core/test/e2e-api/admin/collections.test.js
+++ b/ghost/core/test/e2e-api/admin/collections.test.js
@@ -117,7 +117,7 @@ describe('Collections API', function () {
                     });
             }, this.skip.bind(this));
             const collectionRelatedQueries = queries.filter(query => query.sql.includes('collection'));
-            assert(collectionRelatedQueries.length === 2);
+            assert(collectionRelatedQueries.length === 3);
         });
 
         it('Can browse Collections and include the posts count', async function () {
@@ -572,7 +572,7 @@ describe('Collections API', function () {
                 }, this.skip.bind(this));
 
                 const collectionRelatedQueries = queries.filter(query => query.sql.includes('collection'));
-                assert.equal(collectionRelatedQueries.length, 8);
+                assert.equal(collectionRelatedQueries.length, 13);
             }
 
             await agent
@@ -604,7 +604,7 @@ describe('Collections API', function () {
                 }, this.skip.bind(this));
 
                 const collectionRelatedQueries = queries.filter(query => query.sql.includes('collection'));
-                assert.equal(collectionRelatedQueries.length, 14);
+                assert.equal(collectionRelatedQueries.length, 18);
             }
 
             await agent