2000s
Billingsley played Dr. John Fallow in a West Wing episode that featured the Gall–Peters projection map (season 2, episode 16). He was cast as Professor Miles Ballard in the short-lived television series The Others; then as the Denobulan Doctor Phlox in the fifth live-action Star Trek series, Star Trek: Enterprise, which ran for four seasons. He also played himself in an episode of Roswell that used the Enterprise set. He also starred in the independent film Breathing Hard (2000) in the same year. In 2002, he was a guest star in an episode of Stargate SG-1, playing a scientist who is also a Trekkie, "worshipping at the altar of Roddenberry". He played a supporting role in the 2003 thriller Out of Time as medical examiner and best friend to the chief of police, played by Denzel Washington.
Billingsley is well known to fans of the series Cold Case for his guest appearance in the show's second season, playing serial killer George Marks, the only killer on the show to get away with murder. He reprised the role in the season finale, in which Marks was killed. He also appeared as a blunt-force victim in the first season of Six Feet Under, in the episode "The New Person".
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, as well as the 2017 sequel The Man from Earth: Holocene. 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.
Billingsley appeared as Jacob Nolston in "Crash Into Me", a two-part, fourth-season episode of the TV drama Grey's Anatomy.
Billingsley and his wife have also appeared as themselves on the HGTV series My House Is Worth What?, in which a real estate expert toured their home and provided commentary for viewers before providing an appraisal.
In 2008, Billingsley had a supporting role in several episodes of the HBO series True Blood as coroner Mike Spencer. In May of that year, he guest starred as John Harris, the father of the Kiss-Me-Not Killer, in "Never Tell", an episode of Women's Murder Club.
He appeared in the disaster film 2012, which was released on November 13, 2009, as Professor Frederic West, an American scientist. He subsequently appeared on the ABC series Scrubs in December 2009.