After graduating from NYU, Dowdle moved to Los Angeles to pursue a career in filmmaking. Dowdle wrote and directed his first feature, the 1996 film Full Moon Rising, when he was just out of college. For his sophomore effort, The Dry Spell, Dowdle was joined by his younger brother Drew, who produced the film as John wrote, directed and edited. They now live in Los Angeles, working together as The Brothers Dowdle.
With his brother Drew Dowdle as a Producer and/or co-screenwriter, John Erick Dowdle directed the horror films Quarantine, Devil, based on a storybook from M. Night Shyamalan, and As Above, So Below, as well as the 2015 thriller film No Escape, starring Owen Wilson and Pierce Brosnan.
In 2017, Dowdle co-created the miniseries Waco with his brother, which is set to air on Paramount Network in 2018.