diff --git a/plugins/commands/cloud/client/client.rb b/plugins/commands/cloud/client/client.rb
index 0e9452e1d..365973706 100644
--- a/plugins/commands/cloud/client/client.rb
+++ b/plugins/commands/cloud/client/client.rb
@@ -18,6 +18,7 @@ module VagrantPlugins
       ######################################################################
       APP = "app".freeze
 
+      include Util
       include Vagrant::Util::Presence
 
       attr_accessor :client
@@ -32,7 +33,10 @@ module VagrantPlugins
       def initialize(env)
         @logger = Log4r::Logger.new("vagrant::cloud::client")
         @env    = env
-        @client = VagrantCloud::Client.new(access_token: token)
+        @client = VagrantCloud::Client.new(
+          access_token: token,
+          url_base: api_server_url
+        )
       end
 
       # Removes the token, effectively logging the user out.
@@ -72,7 +76,10 @@ module VagrantPlugins
             password: password, description: description, code: code)
 
           Vagrant::Util::CredentialScrubber.sensitive(r[:token])
-          @client = VagrantCloud::Client.new(access_token: r[:token])
+          @client = VagrantCloud::Client.new(
+            access_token: r[:token],
+            url_base: api_server_url
+          )
           r[:token]
         end
       end
@@ -106,7 +113,7 @@ module VagrantPlugins
         end
 
         # Reset after we store the token since this is now _our_ token
-        @client = VagrantCloud::Client.new(access_token: token)
+        @client = VagrantCloud::Client.new(access_token: token, url_base: api_server_url)
 
         nil
       end
diff --git a/plugins/commands/cloud/locales/en.yml b/plugins/commands/cloud/locales/en.yml
index 451bd8dbe..713282261 100644
--- a/plugins/commands/cloud/locales/en.yml
+++ b/plugins/commands/cloud/locales/en.yml
@@ -112,7 +112,7 @@ en:
           Failed to update box %{org}/%{box_name}
       whoami:
         read_error: |-
-          Failed to read organization %{org}
+          Failed to locate account information
       provider:
         create_fail: |-
           Failed to create provider %{provider} on box %{org}/%{box_name} for version %{version}
diff --git a/plugins/commands/cloud/util.rb b/plugins/commands/cloud/util.rb
index 355af731d..36856c5ba 100644
--- a/plugins/commands/cloud/util.rb
+++ b/plugins/commands/cloud/util.rb
@@ -5,8 +5,16 @@ module VagrantPlugins
       def api_server_url
         if Vagrant.server_url == Vagrant::DEFAULT_SERVER_URL
           return "#{Vagrant.server_url}/api/v1"
-        else
-          return Vagrant.server_url
+        end
+        begin
+          addr = URI.parse(Vagrant.server_url.to_s)
+          if addr.path.empty? || addr.path.to_s == "/"
+            addr.path = "/api/v1"
+          end
+
+          addr.to_s
+        rescue URI::Error
+          Vagrant.server_url
         end
       end
 
diff --git a/test/unit/plugins/commands/cloud/client_test.rb b/test/unit/plugins/commands/cloud/client_test.rb
index 843d4e93b..c6be8d842 100644
--- a/test/unit/plugins/commands/cloud/client_test.rb
+++ b/test/unit/plugins/commands/cloud/client_test.rb
@@ -101,7 +101,7 @@ describe VagrantPlugins::CloudCommand::Client do
     end
 
     it "should create a new internal client" do
-      expect(VagrantCloud::Client).to receive(:new).with(access_token: new_token)
+      expect(VagrantCloud::Client).to receive(:new).with(access_token: new_token, url_base: anything)
       subject.login
     end
 
@@ -174,7 +174,7 @@ describe VagrantPlugins::CloudCommand::Client do
     end
 
     it "should create a new internal client with token" do
-      expect(VagrantCloud::Client).to receive(:new).with(access_token: new_token)
+      expect(VagrantCloud::Client).to receive(:new).with(access_token: new_token, url_base: anything)
       subject.store_token(new_token)
     end