Tudyk appeared on the sitcom Suburgatory (2011–14) and has had guest roles on many other series. Earlier in his career, he appeared frequently in Broadway plays as well. He wrote, directed, and starred in the comedy web series Con Man (2015–17) about a struggling actor whose career is still defined by a successful science fiction TV show he was once on, loosely based on Tudyk's own experience having been on Firefly. The series aired on Syfy in 2017 and earned him a Primetime Emmy Award nomination.
In 2019, Tudyk plays the main antagonist, Mr. Nobody, in the DC universe series Doom Patrol.