Denton got serious about acting as a student at the University of Tennessee Knoxville, where he earned a degree in advertising. The son of a community theater actor, Denton started with the stage. He worked as a radio ad salesman in Nashville by day and performed theater productions in North Carolina, Chicago and California by night for four years.

Denton eventually moved to Chicago, where he became was a company member at The Griffin Theater and the Strawdog Theater Ensemble. His greatest accolades came for his portrayal of a Kentucky preacher in "The Diviners," which gained him a nomination for a Best Actor "Joseph Jefferson Award", a mark of great repute in the Chicago theater community.

In 1997, Denton joined the cast of NBC’s “The Pretender” (1996-2000). During his four years playing the creepy sociopath, Mr. Lyle, Denton also made appearances on “Sliders”, “JAG”, “Two Guys, a Girl and a Pizza Place” and “Ally McBeal”. And clearly not one to let dust settle on his rising star, Denton also built movie credits with “That Old Feeling” (1997), director John Woo’s “Face/Off” (1997) and as a member of the star-studded cast for the critically acclaimed “Primary Colors” (1998).

After an appearance on “The West Wing” in 2000, producer Steven Bocho cast him opposite Kim Delaney for the second season of “Philly” (ABC, 2001-2002). After guest spots on “The Drew Carey Show” and “JAG”, Denton had a new role was as leader of an elite Homeland Security team in “Threat Matrix” (ABC, 2003).

Next, Denton went from an experienced, but relatively unknown actor who takes in stray animals to the media hype surrounding his turn as the new neighbor with hidden secrets who beguiles Teri Hatcher’s “Desperate” character. The exposure catapulted the former mentor for the Big Brother program onto People magazine’s “Sexiest Man Alive” list in 2004. Country Music Television tapped Denton to host the Miss America pageant, taped in Las Vegas instead of the traditional Atlantic City, in 2006.