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In 2000, he made his television debut on the long-running soap opera All My Children. Bomer graduated from Carnegie Mellon University with a Bachelor of Fine Arts degree. Soon after, he had a contract role on Guiding Light, as well as appearing on primetime shows, including Tru Calling.

In 2005, Bomer made his film debut in the mystery-thriller Flightplan, then in 2007 gained recognition with his recurring role in the NBC television series Chuck. 2009 saw Bomer then land the lead role of con-artist and thief Neal Caffrey in the USA Network series White Collar with the series lasting to 2014. He has featured in supporting roles in 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. In 2015, he won a Golden Globe Award and received a nomination for the Primetime Emmy Award for playing a closeted writer of The New York Times in the drama television film The Normal Heart about the rise of the HIV-AIDS crisis in New York City. Bomer made a guest appearance on the fourth season of FX's horror anthology series American Horror Story. He was later upgraded to the main cast during the fifth season. In 2017 he received praise for his performances in the drama films Walking Out, Anything, and the 2018 comedy-drama Papi Chulo. He portrays Larry Trainor in the DC Universe series Doom Patrol, which premiered in 2019.

On stage, Bomer starred in the Dustin Lance Black play 8 on Broadway, and at the Wilshire Ebell Theatre in Los Angeles as Jeff Zarrillo, a plaintiff in the federal case that overturned California's Proposition 8. In 2018 he starred in revival of the Mart Crowley play The Boys in the Band on Broadway playing Donald; he reprised his role for the 2020 film of the same name.