Billingsley appeared in the first season of the series Prison Break as the mysterious Terrence Steadman, brother of the Vice President, whose death is faked to frame Lincoln Burrows for murder. Soon after, he was cast as a regular on the series The Nine. This left him unable to continue his role as Steadman, and he was replaced in the role by Jeff Perry. In 2005, he played the voice of Trask in Ultimate Spider-Man. In November 2006, Billingsley portrayed william Bradford on two episodes of the podcast The Radio Adventures of Dr. Floyd. In May 2007 he appeared on NCIS as a blind Photographer in the episode, "In The Dark". He appeared in the seventh season of 24 as a recurring character. On October 8, 2007, he also made a guest appearance on Journeyman as Alan Platt. Billingsley played Prof. Harry, a Biologist, in the 2007 independent science fiction film The Man from Earth. He also made a guest appearance in an October 2007 episode of CSI: Crime Scene Investigation, and in 2006 on the spinoff series CSI: NY.