With his parents driving him the 90 miles to Los Angeles for auditions and jobs, he worked as a child actor as a young teenager.
In 2000, Handley starred in the Disney Channel Original Movie, Phantom of the Megaplex.
Also in 2007, Handley starred as Johnny Miller in the short-lived series Hidden Palms, on The CW.
Handley also co-starred alongside Dennis Quaid in the series Vegas, playing the character Dixon Lamb.
In 2013, he appeared in the commercial "Greatness Awaits" for the PlayStation 4 console, and in 2020 in the State Farm Insurance commercial "Not the One", in which he played a rejected contestant from a Bachelorette-esque program who is comforted by "Jake from State Farm".