diff --git a/app/controllers/autocomplete_controller.rb b/app/controllers/autocomplete_controller.rb
index 3766b64a09154caecd497c0ef7cecfea51e8b3b4..0d5c8657c9eba40280b83fbd3d76e8df9060f01f 100644
--- a/app/controllers/autocomplete_controller.rb
+++ b/app/controllers/autocomplete_controller.rb
@@ -20,7 +20,7 @@ class AutocompleteController < ApplicationController
   end
 
   def user
-    user = UserFinder.new(params).execute!
+    user = UserFinder.new(params[:id]).find_by_id!
 
     render json: UserSerializer.new.represent(user)
   end
diff --git a/app/controllers/profiles/keys_controller.rb b/app/controllers/profiles/keys_controller.rb
index 01801c313276ee2eabc01d063536e0372d39ebf1..3c3dc03a4eefe4a9e1bc818fa09cbb2e9c046d3d 100644
--- a/app/controllers/profiles/keys_controller.rb
+++ b/app/controllers/profiles/keys_controller.rb
@@ -38,7 +38,7 @@ class Profiles::KeysController < Profiles::ApplicationController
   def get_keys
     if params[:username].present?
       begin
-        user = User.find_by_username(params[:username])
+        user = UserFinder.new(params[:username]).find_by_username
         if user.present?
           render text: user.all_ssh_keys.join("\n"), content_type: "text/plain"
         else
diff --git a/app/controllers/snippets_controller.rb b/app/controllers/snippets_controller.rb
index 694c3a59e2b77c4ab15a0d748ac64bb65b9e0e5e..dd9bf17cf0c7fc2a49c16a7b6b2de80a07fb1e77 100644
--- a/app/controllers/snippets_controller.rb
+++ b/app/controllers/snippets_controller.rb
@@ -26,12 +26,9 @@ class SnippetsController < ApplicationController
   layout 'snippets'
   respond_to :html
 
-  # rubocop: disable CodeReuse/ActiveRecord
   def index
     if params[:username].present?
-      @user = User.find_by(username: params[:username])
-
-      return render_404 unless @user
+      @user = UserFinder.new(params[:username]).find_by_username!
 
       @snippets = SnippetsFinder.new(current_user, author: @user, scope: params[:scope])
         .execute.page(params[:page])
@@ -41,7 +38,6 @@ class SnippetsController < ApplicationController
       redirect_to(current_user ? dashboard_snippets_path : explore_snippets_path)
     end
   end
-  # rubocop: enable CodeReuse/ActiveRecord
 
   def new
     @snippet = PersonalSnippet.new
diff --git a/app/finders/issuable_finder.rb b/app/finders/issuable_finder.rb
index 1f98ecf95ca0304f0707816e7ae9db65ce731a00..8abfe0c4c176887678419681fe1b3bd5955473d9 100644
--- a/app/finders/issuable_finder.rb
+++ b/app/finders/issuable_finder.rb
@@ -256,7 +256,7 @@ class IssuableFinder
       if assignee_id?
         User.find_by(id: params[:assignee_id])
       elsif assignee_username?
-        User.find_by(username: params[:assignee_username])
+        User.find_by_username(params[:assignee_username])
       else
         nil
       end
@@ -284,7 +284,7 @@ class IssuableFinder
       if author_id?
         User.find_by(id: params[:author_id])
       elsif author_username?
-        User.find_by(username: params[:author_username])
+        User.find_by_username(params[:author_username])
       else
         nil
       end
diff --git a/app/finders/user_finder.rb b/app/finders/user_finder.rb
index 815388c894ef584108d1299ba86030c72439f8b5..556be4c4338cb9e9bc75c42d725772fd6d50f551 100644
--- a/app/finders/user_finder.rb
+++ b/app/finders/user_finder.rb
@@ -7,22 +7,52 @@
 # times we may want to exclude blocked user. By using this finder (and extending
 # it whenever necessary) we can keep this logic in one place.
 class UserFinder
-  attr_reader :params
+  def initialize(username_or_id)
+    @username_or_id = username_or_id
+  end
+
+  # Tries to find a User by id, returning nil if none could be found.
+  def find_by_id
+    User.find_by_id(@username_or_id)
+  end
 
-  def initialize(params)
-    @params = params
+  # Tries to find a User by id, raising a `ActiveRecord::RecordNotFound` if it could
+  # not be found.
+  def find_by_id!
+    User.find(@username_or_id)
   end
 
-  # Tries to find a User, returning nil if none could be found.
-  # rubocop: disable CodeReuse/ActiveRecord
-  def execute
-    User.find_by(id: params[:id])
+  # Tries to find a User by username, returning nil if none could be found.
+  def find_by_username
+    User.find_by_username(@username_or_id)
   end
-  # rubocop: enable CodeReuse/ActiveRecord
 
-  # Tries to find a User, raising a `ActiveRecord::RecordNotFound` if it could
+  # Tries to find a User by username, raising a `ActiveRecord::RecordNotFound` if it could
   # not be found.
-  def execute!
-    User.find(params[:id])
+  def find_by_username!
+    User.find_by_username!(@username_or_id)
+  end
+
+  # Tries to find a User by username or id, returning nil if none could be found.
+  def find_by_id_or_username
+    if input_is_id?
+      find_by_id
+    else
+      find_by_username
+    end
+  end
+
+  # Tries to find a User by username or id, raising a `ActiveRecord::RecordNotFound` if it could
+  # not be found.
+  def find_by_id_or_username!
+    if input_is_id?
+      find_by_id!
+    else
+      find_by_username!
+    end
+  end
+
+  def input_is_id?
+    @username_or_id.is_a?(Numeric) || @username_or_id =~ /^\d+$/
   end
 end
diff --git a/app/finders/users_finder.rb b/app/finders/users_finder.rb
index f2ad9b4bda5ee2166f02cd617fb9c50989203cdf..81ae50c0bd1fb714a446e883d6e345057bc4e4a3 100644
--- a/app/finders/users_finder.rb
+++ b/app/finders/users_finder.rb
@@ -43,13 +43,11 @@ class UsersFinder
 
   private
 
-  # rubocop: disable CodeReuse/ActiveRecord
   def by_username(users)
     return users unless params[:username]
 
-    users.where(username: params[:username])
+    users.by_username(params[:username])
   end
-  # rubocop: enable CodeReuse/ActiveRecord
 
   def by_search(users)
     return users unless params[:search].present?
diff --git a/app/models/user.rb b/app/models/user.rb
index a0665518cf5b6669689a2f79d6e87f6b90f64215..34efb22b35982a57b290a438e9415ff346cf67f2 100644
--- a/app/models/user.rb
+++ b/app/models/user.rb
@@ -264,7 +264,7 @@ class User < ActiveRecord::Base
   scope :order_recent_sign_in, -> { reorder(Gitlab::Database.nulls_last_order('current_sign_in_at', 'DESC')) }
   scope :order_oldest_sign_in, -> { reorder(Gitlab::Database.nulls_last_order('current_sign_in_at', 'ASC')) }
   scope :confirmed, -> { where.not(confirmed_at: nil) }
-  scope :by_username, -> (usernames) { iwhere(username: usernames) }
+  scope :by_username, -> (usernames) { iwhere(username: Array(usernames).map(&:to_s)) }
   scope :for_todos, -> (todos) { where(id: todos.select(:user_id)) }
 
   # Limits the users to those that have TODOs, optionally in the given state.
diff --git a/bin/profile-url b/bin/profile-url
index d8d096416249cfe1ad1225fd777e50682d3d33f3..9e8585aabba8f5af1a6bf284a14d5d493a1b7d02 100755
--- a/bin/profile-url
+++ b/bin/profile-url
@@ -48,7 +48,7 @@ require File.expand_path('../config/environment', File.dirname(__FILE__))
 result = Gitlab::Profiler.profile(options[:url],
                                   logger: Logger.new(options[:sql_output]),
                                   post_data: options[:post_data],
-                                  user: User.find_by_username(options[:username]),
+                                  user: UserFinder.new(options[:username]).find_by_username,
                                   private_token: ENV['PRIVATE_TOKEN'])
 
 printer = RubyProf::CallStackPrinter.new(result)
diff --git a/changelogs/unreleased/38304-username-API-call-case-sensitive.yml b/changelogs/unreleased/38304-username-API-call-case-sensitive.yml
new file mode 100644
index 0000000000000000000000000000000000000000..b89778b6c239116d99f8a01d4c6a4f864d3ca4de
--- /dev/null
+++ b/changelogs/unreleased/38304-username-API-call-case-sensitive.yml
@@ -0,0 +1,5 @@
+---
+title: "Use case insensitve username lookups"
+merge_request: 21728
+author: William George
+type: fixed
\ No newline at end of file
diff --git a/doc/api/README.md b/doc/api/README.md
index a351db99bbdabbeaa62772c46266a701f1840ca6..ec539e2d044415ee9e321e8bf6b437e4aa364558 100644
--- a/doc/api/README.md
+++ b/doc/api/README.md
@@ -233,7 +233,10 @@ provided you are authenticated as an administrator with an OAuth or Personal Acc
 
 You need to pass the `sudo` parameter either via query string or a header with an ID/username of
 the user you want to perform the operation as. If passed as a header, the
-header name must be `Sudo`.
+header name must be `Sudo`. 
+
+NOTE: **Note:**
+Usernames are case insensitive.
 
 If a non administrative access token is provided, an error message will
 be returned with status code `403`:
diff --git a/doc/api/users.md b/doc/api/users.md
index 07f03f9c827f937c3fa19d094176b27a27ed9bd1..ee24aa0915664ba9a9080ba71f89dde45d80d114 100644
--- a/doc/api/users.md
+++ b/doc/api/users.md
@@ -59,6 +59,9 @@ GET /users?active=true
 GET /users?blocked=true
 ```
 
+NOTE: **Note:**
+Username search is case insensitive.
+
 ### For admins
 
 ```
diff --git a/lib/api/features.rb b/lib/api/features.rb
index 6f2422af13ae4a79075030611f6e4232e5567488..1331248699fd5794915bb215e5999d97d67cd0a6 100644
--- a/lib/api/features.rb
+++ b/lib/api/features.rb
@@ -20,7 +20,7 @@ module API
       def gate_targets(params)
         targets = []
         targets << Feature.group(params[:feature_group]) if params[:feature_group]
-        targets << User.find_by_username(params[:user]) if params[:user]
+        targets << UserFinder.new(params[:user]).find_by_username if params[:user]
 
         targets
       end
diff --git a/lib/api/helpers.rb b/lib/api/helpers.rb
index a7ba80662339b9b60e96981ae7c065ea7bc04473..60bf977f0e4d7b2d0cddb88cda3fbc1e5e829fd0 100644
--- a/lib/api/helpers.rb
+++ b/lib/api/helpers.rb
@@ -96,15 +96,9 @@ module API
       LabelsFinder.new(current_user, search_params).execute
     end
 
-    # rubocop: disable CodeReuse/ActiveRecord
     def find_user(id)
-      if id =~ /^\d+$/
-        User.find_by(id: id)
-      else
-        User.find_by(username: id)
-      end
+      UserFinder.new(id).find_by_id_or_username
     end
-    # rubocop: enable CodeReuse/ActiveRecord
 
     # rubocop: disable CodeReuse/ActiveRecord
     def find_project(id)
diff --git a/lib/api/internal.rb b/lib/api/internal.rb
index 6a264c4cc6d4b1673baf6050f48162f5963be357..4dd6b19e3536e7357ddd22671336f3f4a87633d0 100644
--- a/lib/api/internal.rb
+++ b/lib/api/internal.rb
@@ -40,7 +40,7 @@ module API
           elsif params[:user_id]
             User.find_by(id: params[:user_id])
           elsif params[:username]
-            User.find_by_username(params[:username])
+            UserFinder.new(params[:username]).find_by_username
           end
 
         protocol = params[:protocol]
@@ -154,7 +154,7 @@ module API
         elsif params[:user_id]
           user = User.find_by(id: params[:user_id])
         elsif params[:username]
-          user = User.find_by(username: params[:username])
+          user = UserFinder.new(params[:username]).find_by_username
         end
 
         present user, with: Entities::UserSafe
diff --git a/lib/api/users.rb b/lib/api/users.rb
index 501c5cf1df33bc25e4e15a1fe75d62b2e8b577dd..47382b092074cb3e4c6a4de2323b250da2869c15 100644
--- a/lib/api/users.rb
+++ b/lib/api/users.rb
@@ -155,7 +155,6 @@ module API
         requires :username, type: String, desc: 'The username of the user'
         use :optional_attributes
       end
-      # rubocop: disable CodeReuse/ActiveRecord
       post do
         authenticated_as_admin!
 
@@ -166,17 +165,16 @@ module API
           present user, with: Entities::UserPublic, current_user: current_user
         else
           conflict!('Email has already been taken') if User
-              .where(email: user.email)
-              .count > 0
+            .by_any_email(user.email.downcase)
+            .any?
 
           conflict!('Username has already been taken') if User
-              .where(username: user.username)
-              .count > 0
+            .by_username(user.username)
+            .any?
 
           render_validation_error!(user)
         end
       end
-      # rubocop: enable CodeReuse/ActiveRecord
 
       desc 'Update a user. Available only for admins.' do
         success Entities::UserPublic
@@ -198,11 +196,11 @@ module API
         not_found!('User') unless user
 
         conflict!('Email has already been taken') if params[:email] &&
-            User.where(email: params[:email])
+            User.by_any_email(params[:email].downcase)
                 .where.not(id: user.id).count > 0
 
         conflict!('Username has already been taken') if params[:username] &&
-            User.where(username: params[:username])
+            User.by_username(params[:username])
                 .where.not(id: user.id).count > 0
 
         user_params = declared_params(include_missing: false)
diff --git a/lib/gitlab/google_code_import/importer.rb b/lib/gitlab/google_code_import/importer.rb
index 94c1573923164db42c1653eee3a05887db3e5853..0c08c0fedaa704f073fb8d26cfe6fdeea6721499 100644
--- a/lib/gitlab/google_code_import/importer.rb
+++ b/lib/gitlab/google_code_import/importer.rb
@@ -102,7 +102,7 @@ module Gitlab
             if username.start_with?("@")
               username = username[1..-1]
 
-              if user = User.find_by(username: username)
+              if user = UserFinder.new(username).find_by_username
                 assignee_id = user.id
               end
             end
diff --git a/lib/gitlab/metrics/influx_db.rb b/lib/gitlab/metrics/influx_db.rb
index 04135dac4ff5a0cfdd7f7c864d6592e5534f607d..ce9d3ec3de485f3593880f610786d6765156fc34 100644
--- a/lib/gitlab/metrics/influx_db.rb
+++ b/lib/gitlab/metrics/influx_db.rb
@@ -86,7 +86,7 @@ module Gitlab
         # Example:
         #
         #     Gitlab::Metrics.measure(:find_by_username_duration) do
-        #       User.find_by_username(some_username)
+        #       UserFinder.new(some_username).find_by_username
         #     end
         #
         # name - The name of the field to store the execution time in.
diff --git a/lib/tasks/import.rake b/lib/tasks/import.rake
index fc59b3f937d53ba500218ee56be3c891d6bdba32..a16d4c47273fd0746b40c3cb5b0f18a7ab0d152e 100644
--- a/lib/tasks/import.rake
+++ b/lib/tasks/import.rake
@@ -9,7 +9,7 @@ class GithubImport
   def initialize(token, gitlab_username, project_path, extras)
     @options = { token: token }
     @project_path = project_path
-    @current_user = User.find_by(username: gitlab_username)
+    @current_user = UserFinder.new(gitlab_username).find_by_username
 
     raise "GitLab user #{gitlab_username} not found. Please specify a valid username." unless @current_user
 
diff --git a/spec/finders/user_finder_spec.rb b/spec/finders/user_finder_spec.rb
index e53aa50dd33d8871d36b21da385b5d1ba2d8ed34..4771b878b8e53281cd83f6886048cd85b152c103 100644
--- a/spec/finders/user_finder_spec.rb
+++ b/spec/finders/user_finder_spec.rb
@@ -3,40 +3,176 @@
 require 'spec_helper'
 
 describe UserFinder do
-  describe '#execute' do
+  set(:user) { create(:user) }
+
+  describe '#find_by_id' do
+    context 'when the user exists' do
+      it 'returns the user' do
+        found = described_class.new(user.id).find_by_id
+
+        expect(found).to eq(user)
+      end
+    end
+
+    context 'when the user exists (id as string)' do
+      it 'returns the user' do
+        found = described_class.new(user.id.to_s).find_by_id
+
+        expect(found).to eq(user)
+      end
+    end
+
+    context 'when the user does not exist' do
+      it 'returns nil' do
+        found = described_class.new(1).find_by_id
+
+        expect(found).to be_nil
+      end
+    end
+  end
+
+  describe '#find_by_username' do
     context 'when the user exists' do
       it 'returns the user' do
-        user = create(:user)
-        found = described_class.new(id: user.id).execute
+        found = described_class.new(user.username).find_by_username
+
+        expect(found).to eq(user)
+      end
+    end
+
+    context 'when the user does not exist' do
+      it 'returns nil' do
+        found = described_class.new("non_existent_username").find_by_username
+
+        expect(found).to be_nil
+      end
+    end
+  end
+
+  describe '#find_by_id_or_username' do
+    context 'when the user exists (id)' do
+      it 'returns the user' do
+        found = described_class.new(user.id).find_by_id_or_username
+
+        expect(found).to eq(user)
+      end
+    end
+
+    context 'when the user exists (id as string)' do
+      it 'returns the user' do
+        found = described_class.new(user.id.to_s).find_by_id_or_username
 
         expect(found).to eq(user)
       end
     end
 
+    context 'when the user exists (username)' do
+      it 'returns the user' do
+        found = described_class.new(user.username).find_by_id_or_username
+
+        expect(found).to eq(user)
+      end
+    end
+
+    context 'when the user does not exist (username)' do
+      it 'returns nil' do
+        found = described_class.new("non_existent_username").find_by_id_or_username
+
+        expect(found).to be_nil
+      end
+    end
+
     context 'when the user does not exist' do
       it 'returns nil' do
-        found = described_class.new(id: 1).execute
+        found = described_class.new(1).find_by_id_or_username
 
         expect(found).to be_nil
       end
     end
   end
 
-  describe '#execute!' do
+  describe '#find_by_id!' do
+    context 'when the user exists' do
+      it 'returns the user' do
+        found = described_class.new(user.id).find_by_id!
+
+        expect(found).to eq(user)
+      end
+    end
+
+    context 'when the user exists (id as string)' do
+      it 'returns the user' do
+        found = described_class.new(user.id.to_s).find_by_id!
+
+        expect(found).to eq(user)
+      end
+    end
+
+    context 'when the user does not exist' do
+      it 'raises ActiveRecord::RecordNotFound' do
+        finder = described_class.new(1)
+
+        expect { finder.find_by_id! }.to raise_error(ActiveRecord::RecordNotFound)
+      end
+    end
+  end
+
+  describe '#find_by_username!' do
     context 'when the user exists' do
       it 'returns the user' do
-        user = create(:user)
-        found = described_class.new(id: user.id).execute!
+        found = described_class.new(user.username).find_by_username!
+
+        expect(found).to eq(user)
+      end
+    end
+
+    context 'when the user does not exist' do
+      it 'raises ActiveRecord::RecordNotFound' do
+        finder = described_class.new("non_existent_username")
+
+        expect { finder.find_by_username! }.to raise_error(ActiveRecord::RecordNotFound)
+      end
+    end
+  end
+
+  describe '#find_by_id_or_username!' do
+    context 'when the user exists (id)' do
+      it 'returns the user' do
+        found = described_class.new(user.id).find_by_id_or_username!
+
+        expect(found).to eq(user)
+      end
+    end
+
+    context 'when the user exists (id as string)' do
+      it 'returns the user' do
+        found = described_class.new(user.id.to_s).find_by_id_or_username!
 
         expect(found).to eq(user)
       end
     end
 
+    context 'when the user exists (username)' do
+      it 'returns the user' do
+        found = described_class.new(user.username).find_by_id_or_username!
+
+        expect(found).to eq(user)
+      end
+    end
+
+    context 'when the user does not exist (username)' do
+      it 'raises ActiveRecord::RecordNotFound' do
+        finder = described_class.new("non_existent_username")
+
+        expect { finder.find_by_id_or_username! }.to raise_error(ActiveRecord::RecordNotFound)
+      end
+    end
+
     context 'when the user does not exist' do
       it 'raises ActiveRecord::RecordNotFound' do
-        finder = described_class.new(id: 1)
+        finder = described_class.new(1)
 
-        expect { finder.execute! }.to raise_error(ActiveRecord::RecordNotFound)
+        expect { finder.find_by_id_or_username! }.to raise_error(ActiveRecord::RecordNotFound)
       end
     end
   end
diff --git a/spec/finders/users_finder_spec.rb b/spec/finders/users_finder_spec.rb
index 4249c52c481e9415da4ba094ceebf51b5ec622e3..fecf97dc64114d0984e7c000f5d3994c4294a6dc 100644
--- a/spec/finders/users_finder_spec.rb
+++ b/spec/finders/users_finder_spec.rb
@@ -22,6 +22,12 @@ describe UsersFinder do
         expect(users).to contain_exactly(user1)
       end
 
+      it 'filters by username (case insensitive)' do
+        users = described_class.new(user, username: 'joHNdoE').execute
+
+        expect(users).to contain_exactly(user1)
+      end
+
       it 'filters by search' do
         users = described_class.new(user, search: 'orando').execute
 
diff --git a/spec/requests/api/helpers_spec.rb b/spec/requests/api/helpers_spec.rb
index 0a789d58fd8125c737f0ea5c79b29e7fa8b3d415..cca449e9e56e859badd27202ca26adb03f9a9e48 100644
--- a/spec/requests/api/helpers_spec.rb
+++ b/spec/requests/api/helpers_spec.rb
@@ -368,6 +368,14 @@ describe API::Helpers do
                 it_behaves_like 'successful sudo'
               end
 
+              context 'when providing username (case insensitive)' do
+                before do
+                  env[API::Helpers::SUDO_HEADER] = user.username.upcase
+                end
+
+                it_behaves_like 'successful sudo'
+              end
+
               context 'when providing user ID' do
                 before do
                   env[API::Helpers::SUDO_HEADER] = user.id.to_s
@@ -386,6 +394,14 @@ describe API::Helpers do
                 it_behaves_like 'successful sudo'
               end
 
+              context 'when providing username (case insensitive)' do
+                before do
+                  set_param(API::Helpers::SUDO_PARAM, user.username.upcase)
+                end
+
+                it_behaves_like 'successful sudo'
+              end
+
               context 'when providing user ID' do
                 before do
                   set_param(API::Helpers::SUDO_PARAM, user.id.to_s)
diff --git a/spec/requests/api/users_spec.rb b/spec/requests/api/users_spec.rb
index 09c1d01608159adae66c909bb71fb556eada948e..e6d01c9689f08a071d5b0c683cde94a0f2a6a9cc 100644
--- a/spec/requests/api/users_spec.rb
+++ b/spec/requests/api/users_spec.rb
@@ -51,6 +51,15 @@ describe API::Users do
         expect(json_response[0]['username']).to eq(user.username)
       end
 
+      it "returns the user when a valid `username` parameter is passed (case insensitive)" do
+        get api("/users"), username: user.username.upcase
+
+        expect(response).to match_response_schema('public_api/v4/user/basics')
+        expect(json_response.size).to eq(1)
+        expect(json_response[0]['id']).to eq(user.id)
+        expect(json_response[0]['username']).to eq(user.username)
+      end
+
       it "returns an empty response when an invalid `username` parameter is passed" do
         get api("/users"), username: 'invalid'
 
@@ -132,6 +141,14 @@ describe API::Users do
         expect(json_response.first['username']).to eq(omniauth_user.username)
       end
 
+      it "returns one user (case insensitive)" do
+        get api("/users?username=#{omniauth_user.username.upcase}", user)
+
+        expect(response).to match_response_schema('public_api/v4/user/basics')
+        expect(response).to include_pagination_headers
+        expect(json_response.first['username']).to eq(omniauth_user.username)
+      end
+
       it "returns a 403 when non-admin user searches by external UID" do
         get api("/users?extern_uid=#{omniauth_user.identities.first.extern_uid}&provider=#{omniauth_user.identities.first.provider}", user)
 
@@ -343,6 +360,12 @@ describe API::Users do
         let(:path) { "/users/#{user.username}/status" }
       end
     end
+
+    context 'when finding the user by username (case insensitive)' do
+      it_behaves_like 'rendering user status' do
+        let(:path) { "/users/#{user.username.upcase}/status" }
+      end
+    end
   end
 
   describe "POST /users" do
@@ -528,6 +551,18 @@ describe API::Users do
         expect(json_response['message']).to eq('Username has already been taken')
       end
 
+      it 'returns 409 conflict error if same username exists (case insensitive)' do
+        expect do
+          post api('/users', admin),
+               name: 'foo',
+               email: 'foo@example.com',
+               password: 'password',
+               username: 'TEST'
+        end.to change { User.count }.by(0)
+        expect(response).to have_gitlab_http_status(409)
+        expect(json_response['message']).to eq('Username has already been taken')
+      end
+
       it 'creates user with new identity' do
         post api("/users", admin), attributes_for(:user, provider: 'github', extern_uid: '67890')
 
@@ -749,6 +784,14 @@ describe API::Users do
         expect(response).to have_gitlab_http_status(409)
         expect(@user.reload.username).to eq(@user.username)
       end
+
+      it 'returns 409 conflict error if username taken (case insensitive)' do
+        @user_id = User.all.last.id
+        put api("/users/#{@user.id}", admin), username: 'TEST'
+
+        expect(response).to have_gitlab_http_status(409)
+        expect(@user.reload.username).to eq(@user.username)
+      end
     end
   end