A year later, he appeared in the episode Bellport in the prime–time soap opera North Shore, the episode was directed by Patrick Norris and aired on September 27 2004, his participation was not credited.In the slasher film The Texas Chainsaw Massacre: The Beginning (2006), the film's story takes place four years before the timeline of the 2003 film, directed by Jonathan Liebesman, Bomer portrayed Eric, a Vietnam War veteran who is driving across Texas to re-enlist after his brother is drafted.

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His character Bryce Larkin, was also a CIA agent, the series in its first season had very positive critics.

In 2007, Bomer took on the role of Ernest Hemingway in a Williamstown Theatre Festival production of Crispin Whittell's play Villa America in Massachusetts, starring with Jennifer Mudge and Nate Corddry. In 2009, he starred in the police procedural—drama series White Collar (2009–2014), opposite Tim De Kay, Willie Garson and Tiffani Thiessen, created by Jeff Eastin, which chronicles the partnership between a con artist, Neal Caffrey and an FBI agent, Peter Burke (De Kay).

He made his television debut with Guiding Light in 2001, and gained recognition with his recurring role in the NBC television series Chuck.

He played the lead role of con-artist and thief Neal Caffrey in the USA Network series White Collar from 2009 to 2014.

The film is loosely based on the youth of the movie's protagonist, Channing Tatum, who worked as a stripper before signing on as an actor.

Also in 2012, now on television, Bomer appears in episode Big Brother of the drama—comedy series Glee. He played Cooper Anderson, Blaine Anderson's older brother (played by Darren Criss).He was later upgraded to main cast during the fifth season.In film, Bomer has featured in supporting roles in the 2005 thriller Flightplan, the 2011 science fiction thriller In Time, the 2012 comedy-drama Magic Mike and its 2015 sequel, the 2014 supernatural-drama Winter's Tale, and the 2016 neo-noir film The Nice Guys.He had a supporting role in the NBC action-comedy–spy–drama Chuck (2007–09), created by Josh Schwartz and Chris Fedak.The series is about an "average computer-whiz-next-door" named Chuck Bartowski (played by Zachary Levi), who receives an encoded e-mail from an old college friend now working for the Central Intelligence Agency (CIA).The brothers run afoul of Sheriff Hoyt and are taken captive by the Hewitt family.