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Denton was born in Nashville, Tennessee and grew up in Goodlettsville, Tennessee, the son of J. T. Denton, a dentist who served in the military. He attended the University of Tennessee where he was a member of the Sigma Alpha Epsilon fraternity, majored in television/journalism and earned a degree in advertising. Before he became an actor, he sold advertising for two radio stations. He began acting at 23, at a community theater in Nashville. He eventually moved to California to become a full time actor.

He is a regular cast member on the television show Desperate Housewives, where he plays the role of Mike Delfino, a plumber who lives on Wisteria Lane and husband of Susan Mayer. He had previously been a regular on several television series, including The Pretender, JAG, Philly, The Drew Carey Show, Reba and Threat Matrix. As well he has guested on Sliders, Two Guys, a Girl and a Pizza Place, Ally McBeal and The West Wing.

He also appeared in two movies, Primary Colors and Face/Off, as well as appearing in the TV movie Custody which aired in September 2007.

He performed with Band from TV along with Hugh Laurie, Brad Savage, Larry Thomas, among others.

Denton has been married twice. He and his first wife, Jenna Lyn Ward, also an actress, were married from 1997-2000. He got married for the second time on December 16, 2002 to Erin O'Brien. He has two children with his wife Erin, a son named Sheppard born in March 2003, and a daughter Malin O'Brien, born March 22, 2005. He is known to be an Los Angeles Dodgers baseball fan and often attends games. He is also part of the owners group of an independent minor league baseball team in Fullerton, the Orange County Flyers, part of the Golden Baseball League. He is at almost all of the games.