After graduating from college, Miller moved out to Los Angeles where he began working in the mail room of Industry Entertainment. His first break into acting came after he signed on with the Wilhelmina modeling agency. He appeared in six commercials, including two for Electronic Arts' The Sims. He also did commercials for JCPenney, Pizza Hut and pokerparty.com. At the age of 24, Miller screen-tested for the CBSDaytime soap operaAs the World Turns, but due to bad management, he lost the audition, and subsequently the management and agency. He took a two-year hiatus from acting after that experience. In 2006, Miller returned to acting, starring in an episode of . A year later, he landed the role of Richie Novak, the murdering and blackmailing brother of Annie Lavery on the ABC Daytime soap opera All My Children. His first on-screen appearance was August 30, 2007. When news of the character's demise broke in August 2008, Miller began the audition process again. Barbara Bloom, Julie Hanan Carruthers, Marla Kanelos, and screen-test partners Peter Bergman and Elizabeth Hendrickson were instrumental in helping him get the job at The Young and the Restless. Miller's last appearance as Richie Novak on All My Children coincided with his first appearance as Billy Abbott on The Young and the Restless on September 19, 2008. He became the fourth contract actor to fill the role, a role that had been met with varying degrees of success in its three previous attempts to recast the part. Miller, who submitted the longest Emmy reel among all nominated performers, was awarded for his work in an It's A Wonderful Life-styled episode of The Young and the Restless with his first nomination and win as Outstanding Supporting Actor in a Drama Series on June 27, 2010 as well as June 14, 2013. In 2011, he was nominated a second time in the Outstanding Supporting Actor category for the same role. Miller also appears, as himself, in an independent film titled Remembering Nigel, which premiered at the Paso RoblesDigital Film Festival on November 25, 2009. In August 2012, it was confirmed that Miller would be appearing in primetime as a recurring cast member on the CW Network’s thriller Ringer. Miller was also cast as Gabe Watson in the Lifetime made-for-TV movieFatal Honeymoon. On September 2, 2014, General Hospitalexecutive producerFrank Valentini announced on Twitter that Miller would join the cast as Jason Morgan. In March 2018, for his portrayal of Jason, Miller earned a nomination for Outstanding Lead Actor. In 2017, with the return of Steve Burton to the role of Jason, Miller's casting was retconned to that of his twin, Drew Cain. In July 2019, Miller announced his exit from the soap.