diff --git a/CHANGELOG.md b/CHANGELOG.md
index 06534b3de..304707bbe 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -3,6 +3,8 @@
 Breaking changes:
 
 Features:
+- [#1618](https://github.com/rails-api/active_model_serializers/issues/1618) Get collection root key for
+  empty collection from explicit serializer option, when possible. (@bf4)
 - [#1574](https://github.com/rails-api/active_model_serializers/pull/1574) Provide key translation. (@remear)
 - [#1494](https://github.com/rails-api/active_model_serializers/pull/1494) Make serializers serializalbe
   (using the Attributes adapter by default). (@bf4)
diff --git a/lib/active_model/serializer.rb b/lib/active_model/serializer.rb
index d78b873fb..79478abb7 100644
--- a/lib/active_model/serializer.rb
+++ b/lib/active_model/serializer.rb
@@ -182,7 +182,7 @@ def as_json(adapter_opts = nil)
 
     # Used by adapter as resource root.
     def json_key
-      root || object.class.model_name.to_s.underscore
+      root || _type || object.class.model_name.to_s.underscore
     end
 
     def read_attribute_for_serialization(attr)
diff --git a/lib/active_model/serializer/collection_serializer.rb b/lib/active_model/serializer/collection_serializer.rb
index ebaded3d7..f026ebfe8 100644
--- a/lib/active_model/serializer/collection_serializer.rb
+++ b/lib/active_model/serializer/collection_serializer.rb
@@ -8,15 +8,10 @@ class CollectionSerializer
       attr_reader :object, :root
 
       def initialize(resources, options = {})
-        @root = options[:root]
-        @object = resources
-
+        @object                  = resources
+        @options                 = options
+        @root                    = options[:root]
         serializer_context_class = options.fetch(:serializer_context_class, ActiveModel::Serializer)
-
-        if resources.blank? && options[:serializer]
-          @each_serializer = options[:serializer]
-        end
-
         @serializers = resources.map do |resource|
           serializer_class = options.fetch(:serializer) { serializer_context_class.serializer_for(resource) }
 
@@ -32,9 +27,28 @@ def success?
         true
       end
 
+      # TODO: unify naming of root, json_key, and _type.  Right now, a serializer's
+      # json_key comes from the root option or the object's model name, by default.
+      # But, if a dev defines a custom `json_key` method with an explicit value,
+      # we have no simple way to know that it is safe to call that instance method.
+      # (which is really a class property at this point, anyhow).
+      # rubocop:disable Metrics/CyclomaticComplexity
+      # Disabling cop since it's good to highlight the complexity of this method by
+      # including all the logic right here.
       def json_key
-        root || derived_root || guess_root || default_root
+        return root if root
+        # 1. get from options[:serializer] for empty resource collection
+        key = object.empty? &&
+          (explicit_serializer_class = options[:serializer]) &&
+          explicit_serializer_class._type
+        # 2. get from first serializer instance in collection
+        key ||= (serializer = serializers.first) && serializer.json_key
+        # 3. get from collection name, if a named collection
+        key ||= object.respond_to?(:name) ? object.name && object.name.underscore : nil
+        # 4. key may be nil for empty collection and no serializer option
+        key && key.pluralize
       end
+      # rubocop:enable Metrics/CyclomaticComplexity
 
       def paginated?
         object.respond_to?(:current_page) &&
@@ -44,21 +58,7 @@ def paginated?
 
       protected
 
-      attr_reader :serializers
-
-      private
-
-      def derived_root
-        serializers.first.try(:json_key).try(:pluralize)
-      end
-
-      def default_root
-        object.try(:name).try(:underscore).try(:pluralize)
-      end
-
-      def guess_root
-        @each_serializer.try(:allocate).try(:json_key).try(:pluralize)
-      end
+      attr_reader :serializers, :options
     end
   end
 end
diff --git a/test/collection_serializer_test.rb b/test/collection_serializer_test.rb
index 833867b03..5e5267e4e 100644
--- a/test/collection_serializer_test.rb
+++ b/test/collection_serializer_test.rb
@@ -3,6 +3,10 @@
 module ActiveModel
   class Serializer
     class CollectionSerializerTest < ActiveSupport::TestCase
+      MessagesSerializer = Class.new(ActiveModel::Serializer) do
+        type 'messages'
+      end
+
       def setup
         @comment = Comment.new
         @post = Post.new
diff --git a/test/fixtures/poro.rb b/test/fixtures/poro.rb
index 7fc59ffa5..c7fb831c8 100644
--- a/test/fixtures/poro.rb
+++ b/test/fixtures/poro.rb
@@ -183,12 +183,6 @@ def json_key
   end
 end
 
-MessagesSerializer = Class.new(ActiveModel::Serializer) do
-  def json_key
-    'messages'
-  end
-end
-
 AlternateBlogSerializer = Class.new(ActiveModel::Serializer) do
   attribute :id
   attribute :name, key: :title