Costikyan was the CEO of Manifesto Games, a start-up devoted to providing a viable path to market for independently developed computer games. He subsequently worked as a consultant for several years before joining Guerillapps as lead game designer in March 2010 to develop its game "Trash Tycoon" for Facebook. In May 2011, he joined Disney Playdom as senior games designer and in January 2014 assumed the same role at Loop Drop. In June 2015, Costikyan joined Boss Fight Entertainment as senior games designer.