In 2006, he starred as FBI negotiator Matt Flannery in the Fox series Standoff, co-starring Rosemarie De Witt, and he was an ad spokesman for Sprint Nextel.
In summer 2007, Livingston appeared on the off-Broadway stage in the world premiere of Neil La Bute's In a Dark Dark House, produced by MCC Theater, with Frederick Weller and Louisa Krause.
Livingston landed his first role in a major film in 1996's Swingers.
He starred as the male lead, Peter Gibbons, in the comedy cult classic Office Space, which co-starred Jennifer Aniston and was written and directed by Mike Judge.
Livingston's first film role was in 1992, in Dolly Parton's Straight Talk.
He moved to Los Angeles and was cast in supporting roles in Some Folks Call it a Sling Blade and The Low Life.
According to the papers obtained by , an alleged hacker has been continuously changing Livingston’s Wikipedia page since May to say he is dating a man named Lee Dennison.
Every time Livingston’s camp corrects the information, the alleged hacker “changes them back almost immediately,” according to the lawsuit.
Livingston, 42, married actress Rosemarie De Witt on November 2, 2009 in San Francisco.The public revelation causes friction between Matt, who doesn't take much seriously and relies on gut instinct, and Emily, an academic who analyzes every move.Their relationship also gets them into major trouble with their boss, Cheryl Carrera, head of the Los Angeles CNU, and raises eyebrows among their CNU colleagues, including intelligence officer Lia Mathers.Rotten Tomatoes gives the film a score of 82% based on 97 reviews.Deputy Police Chief Brenda Johnson runs the Priority Homicide Division of the LAPD with an unorthodox style. Matt Flannery and Emily Lehman are the top-ranked negotiators in the FBI's Crisis Negotiation Unit (CNU).In 2013, Livingston co-starred in the indie comedy Drinking Buddies alongside Olivia Wilde, Jake Johnson and Anna Kendrick.Drinking Buddies received positive reviews from critics.He also appeared as sardonic writer Jack Berger, Carrie's short-term boyfriend in the fifth and sixth seasons of Sex and the City.He guest starred in the episode "TB or Not TB" of House.The show ran from May–July at the Lucille Lortel Theatre in New York City.In November 2007, the indie film Holly told the story of a Vietnamese girl trafficked into the sex trade in Cambodia.