diff --git a/CHANGELOG.md b/CHANGELOG.md
index ea0d772e5..1eab9a8a7 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -26,6 +26,7 @@ Fixes:
 - [#1214](https://github.com/rails-api/active_model_serializers/pull/1214) retrieve the key from the reflection options when building associations (@NullVoxPopuli, @hut8)
 
 Misc:
+- [#1234](https://github.com/rails-api/active_model_serializers/pull/1234) root option no longer handled at serializer level (@beauby)
 - [#1233](https://github.com/rails-api/active_model_serializers/pull/1233) Top-level meta and meta_key options no longer handled at serializer level (@beauby)
 - [#1232](https://github.com/rails-api/active_model_serializers/pull/1232) fields option no longer handled at serializer level (@beauby)
 - [#1178](https://github.com/rails-api/active_model_serializers/pull/1178) env CAPTURE_STDERR=false lets devs see hard failures (@bf4)
diff --git a/lib/active_model/serializable_resource.rb b/lib/active_model/serializable_resource.rb
index da1a772a8..81c0ea1d6 100644
--- a/lib/active_model/serializable_resource.rb
+++ b/lib/active_model/serializable_resource.rb
@@ -1,7 +1,7 @@
 require 'set'
 module ActiveModel
   class SerializableResource
-    ADAPTER_OPTION_KEYS = Set.new([:include, :fields, :adapter, :meta, :meta_key, :links])
+    ADAPTER_OPTION_KEYS = Set.new([:include, :fields, :adapter, :meta, :meta_key, :links, :root])
 
     # Primary interface to composing a resource with a serializer and adapter.
     # @return the serializable_resource, ready for #as_json/#to_json/#serializable_hash.
diff --git a/lib/active_model/serializer.rb b/lib/active_model/serializer.rb
index 27068b621..40d7d2493 100644
--- a/lib/active_model/serializer.rb
+++ b/lib/active_model/serializer.rb
@@ -164,10 +164,6 @@ def initialize(object, options = {})
       end
     end
 
-    def json_key
-      root || object.class.model_name.to_s.underscore
-    end
-
     def attributes
       attributes = self.class._attributes.dup
 
diff --git a/lib/active_model/serializer/adapter/base.rb b/lib/active_model/serializer/adapter/base.rb
index fc06848a9..58410a58e 100644
--- a/lib/active_model/serializer/adapter/base.rb
+++ b/lib/active_model/serializer/adapter/base.rb
@@ -44,10 +44,6 @@ def meta_key
           instance_options.fetch(:meta_key, 'meta'.freeze)
         end
 
-        def root
-          serializer.json_key.to_sym if serializer.json_key
-        end
-
         def include_meta(json)
           json[meta_key] = meta if meta
           json
diff --git a/lib/active_model/serializer/adapter/json.rb b/lib/active_model/serializer/adapter/json.rb
index ab81f5710..021dbf93b 100644
--- a/lib/active_model/serializer/adapter/json.rb
+++ b/lib/active_model/serializer/adapter/json.rb
@@ -15,6 +15,24 @@ def serializable_hash(options = nil)
         def fragment_cache(cached_hash, non_cached_hash)
           ActiveModel::Serializer::Adapter::Json::FragmentCache.new.fragment_cache(cached_hash, non_cached_hash)
         end
+
+        def root
+          root = instance_options.fetch(:root) do
+            if serializer.respond_to?(:each)
+              key =
+                if serializer.first
+                  serializer.first.object.class.model_name
+                else
+                  serializer.object.try(:name)
+                end
+              key.to_s.pluralize
+            else
+              serializer.object.class.model_name.to_s
+            end
+          end
+
+          root.to_s.underscore.to_sym
+        end
       end
     end
   end
diff --git a/lib/active_model/serializer/array_serializer.rb b/lib/active_model/serializer/array_serializer.rb
index f9c91ea9e..114e851f5 100644
--- a/lib/active_model/serializer/array_serializer.rb
+++ b/lib/active_model/serializer/array_serializer.rb
@@ -5,10 +5,9 @@ class ArraySerializer
       include Enumerable
       delegate :each, to: :@serializers
 
-      attr_reader :object, :root
+      attr_reader :object
 
       def initialize(resources, options = {})
-        @root = options[:root]
         @object = resources
         @serializers = resources.map do |resource|
           serializer_context_class = options.fetch(:serializer_context_class, ActiveModel::Serializer)
@@ -22,11 +21,6 @@ def initialize(resources, options = {})
         end
       end
 
-      def json_key
-        key = root || serializers.first.try(:json_key) || object.try(:name).try(:underscore)
-        key.try(:pluralize)
-      end
-
       def paginated?
         object.respond_to?(:current_page) &&
           object.respond_to?(:total_pages) &&
diff --git a/test/action_controller/serialization_test.rb b/test/action_controller/serialization_test.rb
index e9288d564..e357d9ff4 100644
--- a/test/action_controller/serialization_test.rb
+++ b/test/action_controller/serialization_test.rb
@@ -171,7 +171,7 @@ def test_render_array_using_custom_root
         with_adapter :json do
           get :render_array_using_custom_root
         end
-        expected = { custom_roots: [{ name: 'Name 1', description: 'Description 1' }] }
+        expected = { custom_root: [{ name: 'Name 1', description: 'Description 1' }] }
         assert_equal 'application/json', @response.content_type
         assert_equal expected.to_json, @response.body
       end
@@ -181,7 +181,7 @@ def test_render_array_that_is_empty_using_custom_root
           get :render_array_that_is_empty_using_custom_root
         end
 
-        expected = { custom_roots: [] }
+        expected = { custom_root: [] }
         assert_equal 'application/json', @response.content_type
         assert_equal expected.to_json, @response.body
       end
diff --git a/test/adapter/json/array_test.rb b/test/adapter/json/array_test.rb
new file mode 100644
index 000000000..9212d9f4b
--- /dev/null
+++ b/test/adapter/json/array_test.rb
@@ -0,0 +1,78 @@
+require 'test_helper'
+
+module ActiveModel
+  class Serializer
+    module Adapter
+      class Json
+        class ArrayTest < Minitest::Test
+          def setup
+            @comment = Comment.new
+            @post = Post.new
+            @resource = build_named_collection @comment, @post
+          end
+
+          def build_named_collection(*resource)
+            resource.define_singleton_method(:name) { 'MeResource' }
+            resource
+          end
+
+          def test_root_default
+            serializer = ArraySerializer.new([@comment, @post])
+            adapter = Json.new(serializer)
+            assert_equal(:comments, adapter.send(:root))
+          end
+
+          def test_root
+            serializer = ArraySerializer.new([@comment, @post])
+            adapter = Json.new(serializer, root: 'custom_root')
+            assert_equal(:custom_root, adapter.send(:root))
+          end
+
+          def test_root_with_no_serializers
+            serializer = ArraySerializer.new([])
+            adapter = Json.new(serializer, root: 'custom_root')
+            assert_equal(:custom_root, adapter.send(:root))
+          end
+
+          def test_root_with_resource_with_name_and_serializers
+            serializer = ArraySerializer.new(@resource)
+            adapter = Json.new(serializer)
+            assert_equal(:comments, adapter.send(:root))
+          end
+
+          def test_root_with_resource_with_name_and_no_serializers
+            serializer = ArraySerializer.new(build_named_collection)
+            adapter = Json.new(serializer)
+            assert_equal(:me_resources, adapter.send(:root))
+          end
+
+          def test_root_with_resource_with_nil_name_and_no_serializers
+            resource = []
+            resource.define_singleton_method(:name) { nil }
+            serializer = ArraySerializer.new(resource)
+            adapter = Json.new(serializer)
+            assert_equal(:'', adapter.send(:root))
+          end
+
+          def test_root_with_resource_without_name_and_no_serializers
+            serializer = ArraySerializer.new([])
+            adapter = Json.new(serializer)
+            assert_equal(:'', adapter.send(:root))
+          end
+
+          def test_root_with_explicit_root
+            serializer = ArraySerializer.new(@resource)
+            adapter = Json.new(serializer, root: 'custom_root')
+            assert_equal(:custom_root, adapter.send(:root))
+          end
+
+          def test_root_with_explicit_root_and_no_serializers
+            serializer = ArraySerializer.new(build_named_collection)
+            adapter = Json.new(serializer, root: 'custom_root')
+            assert_equal(:custom_root, adapter.send(:root))
+          end
+        end
+      end
+    end
+  end
+end
diff --git a/test/adapter/json/root_test.rb b/test/adapter/json/root_test.rb
new file mode 100644
index 000000000..f690fd72e
--- /dev/null
+++ b/test/adapter/json/root_test.rb
@@ -0,0 +1,27 @@
+require 'test_helper'
+
+module ActiveModel
+  class Serializer
+    module Adapter
+      class Json
+        class RootTest < Minitest::Test
+          def setup
+            @virtual_value = VirtualValue.new(id: 1)
+          end
+
+          def test_overwrite_root
+            serializer = VirtualValueSerializer.new(@virtual_value)
+            adapter = Json.new(serializer, root: 'smth')
+            assert_equal(:smth, adapter.send(:root))
+          end
+
+          def test_underscore_in_root
+            serializer = VirtualValueSerializer.new(@virtual_value)
+            adapter = Json.new(serializer)
+            assert_equal(:virtual_value, adapter.send(:root))
+          end
+        end
+      end
+    end
+  end
+end
diff --git a/test/adapter/json_api/belongs_to_test.rb b/test/adapter/json_api/belongs_to_test.rb
index acf98f4fa..0406a20d4 100644
--- a/test/adapter/json_api/belongs_to_test.rb
+++ b/test/adapter/json_api/belongs_to_test.rb
@@ -38,7 +38,11 @@ def test_includes_post_id
           end
 
           def test_includes_linked_post
-            @adapter = ActiveModel::Serializer::Adapter::JsonApi.new(@serializer, include: [:post])
+            actual = ActiveModel::SerializableResource.new(
+              @comment,
+              adapter: :json_api,
+              include: [:post])
+                     .serializable_hash
             expected = [{
               id: '42',
               type: 'posts',
@@ -52,11 +56,16 @@ def test_includes_linked_post
                 author: { data: { type: 'authors', id: '1' } }
               }
             }]
-            assert_equal expected, @adapter.serializable_hash[:included]
+            assert_equal expected, actual[:included]
           end
 
           def test_limiting_linked_post_fields
-            @adapter = ActiveModel::Serializer::Adapter::JsonApi.new(@serializer, include: [:post], fields: { post: [:title] })
+            actual = ActiveModel::SerializableResource.new(
+              @comment,
+              adapter: :json_api,
+              include: [:post],
+              fields: { post: [:title] })
+                     .serializable_hash
             expected = [{
               id: '42',
               type: 'posts',
@@ -69,7 +78,7 @@ def test_limiting_linked_post_fields
                 author: { data: { type: 'authors', id: '1' } }
               }
             }]
-            assert_equal expected, @adapter.serializable_hash[:included]
+            assert_equal expected, actual[:included]
           end
 
           def test_include_nil_author
diff --git a/test/array_serializer_test.rb b/test/array_serializer_test.rb
index 3141f7131..202100d8b 100644
--- a/test/array_serializer_test.rb
+++ b/test/array_serializer_test.rb
@@ -40,54 +40,6 @@ def test_serializer_option_not_passed_to_each_serializer
 
         refute serializers.first.custom_options.key?(:serializer)
       end
-
-      def test_root_default
-        @serializer = ArraySerializer.new([@comment, @post])
-        assert_equal @serializer.root, nil
-      end
-
-      def test_root
-        expected =  'custom_root'
-        @serializer = ArraySerializer.new([@comment, @post], root: expected)
-        assert_equal @serializer.root, expected
-      end
-
-      def test_root_with_no_serializers
-        expected =  'custom_root'
-        @serializer = ArraySerializer.new([], root: expected)
-        assert_equal @serializer.root, expected
-      end
-
-      def test_json_key
-        assert_equal @serializer.json_key, 'comments'
-      end
-
-      def test_json_key_with_resource_with_name_and_no_serializers
-        serializer = ArraySerializer.new(build_named_collection)
-        assert_equal serializer.json_key, 'me_resources'
-      end
-
-      def test_json_key_with_resource_with_nil_name_and_no_serializers
-        resource = []
-        resource.define_singleton_method(:name) { nil }
-        serializer = ArraySerializer.new(resource)
-        assert_equal serializer.json_key, nil
-      end
-
-      def test_json_key_with_resource_without_name_and_no_serializers
-        serializer = ArraySerializer.new([])
-        assert_equal serializer.json_key, nil
-      end
-
-      def test_json_key_with_root
-        serializer = ArraySerializer.new(@resource, root: 'custom_root')
-        assert_equal serializer.json_key, 'custom_roots'
-      end
-
-      def test_json_key_with_root_and_no_serializers
-        serializer = ArraySerializer.new(build_named_collection, root: 'custom_root')
-        assert_equal serializer.json_key, 'custom_roots'
-      end
     end
   end
 end
diff --git a/test/serializers/root_test.rb b/test/serializers/root_test.rb
deleted file mode 100644
index 03e6ca20f..000000000
--- a/test/serializers/root_test.rb
+++ /dev/null
@@ -1,21 +0,0 @@
-require 'test_helper'
-
-module ActiveModel
-  class Serializer
-    class RootTest < Minitest::Test
-      def setup
-        @virtual_value = VirtualValue.new(id: 1)
-      end
-
-      def test_overwrite_root
-        serializer = VirtualValueSerializer.new(@virtual_value, { root: 'smth' })
-        assert_equal('smth', serializer.json_key)
-      end
-
-      def test_underscore_in_root
-        serializer = VirtualValueSerializer.new(@virtual_value)
-        assert_equal('virtual_value', serializer.json_key)
-      end
-    end
-  end
-end