[2] He worked for John Hancock Insurance as a life insurance agent in Poughkeepsie, New York, while pursuing his acting career, starring in several stage productions around New Paltz, New York.

Denison is most recently known for his role as Lieutenant Andy Flynn in The Closer (2005–2012) and its spin-off Major Crimes (2012–2018).

[4] Afterwards, he starred and guest-starred in several crime movies and television programs, notably as undercover agent John Henry Raglin in Wiseguy (1987–90), The Great Escape II: The Untold Story (1988), City of Hope (1991), as Joey Buttafuoco in The Amy Fisher Story (1993), as John Gotti in Getting Gotti (1994), Criminal Passion (1994), and as head coach Mike George in ESPN's drama series Playmakers (2003).

He had a recurring role as Aldo Burrows on the Fox series Prison Break (2005–2009).

Denison embodied "Government Investor" in the 2011 Frankie Muniz superhero film Pizza Man.