His first jobs were managing theater companies such as New York's Lincoln Center, the Oregon Shakespeare Festival and the Mineola Theater in Long Island. He is a member of the Academy of Motion Picture Arts and Sciences and the Directors Guild of America. Cunningham is best known for creating the Friday the 13th series of horror films, which introduced the fictional mass murderer Jason Voorhees. Of the 12 films in the series, the ones that had Cunningham's involvement were the original, Jason Goes to Hell: The Final Friday, Jason X, Freddy vs. Jason, and the 2009 reboot. He has also produced many horror films, such as the House series and Wes Craven's debut feature, The Last House on the Left. He is the founder and CEO of Crystal Lake Entertainment. Cunningham is set to produce the CW series adaption of Friday the 13th as well as producing Friday the 13th: The Game.