Television
Dennehy's early professional acting career included small guest roles in such 1970s and 1980s series as Kojak, M*A*S*H, Lou Grant, Dallas, Dynasty, and Hunter. He also appeared in an episode of Miami Vice during the 1987–88 season.
Dennehy portrayed Sergeant Ned T. "Frozen Chosen" Coleman in the television movie A Rumor of War (1980) opposite Brad Davis. He continued to appear in such high-profile television films as Skokie (1981), Split Image (1982), Day One (1989), and A Killing in a Small Town (1990) opposite Barbara Hershey. In 1983 he played government informant Edward Partin in Blood Feud about Jimmy Hoffa.He also played the title role in HBO's Teamster Boss: The Jackie Presser Story.
Dennehy had a lead role as fire chief/celebrity dad Leslie "Buddy" Krebs in the short-lived 1982 series Star of the Family. Despite his star power, that show was cancelled after a half-season. He starred in the crime drama Jack Reed TV movies.
Dennehy was nominated for Emmy Awards six times for his television movies. In 1992, he was nominated for Outstanding Lead Actor in a Miniseries or TV Movie for his performance as John Wayne Gacy in To Catch a Killer, and he was nominated that same year in a different category, Outstanding Supporting Actor in a Miniseries or TV Movie, for The Burden of Proof. Dennehy's other Emmy nominations were for his work in A Killing in a Small Town, Murder in the Heartland (1993) and his work in the Showtime cable TV movie Our Fathers (2005), which was about the Roman Catholic Church sex abuse scandal. In 2000, Dennehy was nominated for an Emmy for Outstanding Lead Actor in a Miniseries or TV Movie for a television presentation for his performance as Willy Loman in Arthur Miller's Death of a Salesman which he had performed on Broadway. While not gaining the actor an Emmy win, the performance did, however, win him a Golden Globe Award. He also appeared as a recurring character in the NBC sitcom Just Shoot Me!.
A cartoon version of Dennehy appeared in the 1999 film South Park: Bigger, Longer & Uncut as well as in an episode of The Simpsons.
In January 2007, he starred in the episode "Scheherazade" of Law & Order: Special Victims Unit as a retired criminal who wants to reconnect with his daughter and admit his crimes before dying of a terminal disease thus eventually clearing a wrongfully imprisoned inmate. In April 2008, Dennehy guest-starred as a Teamster boss in "Sandwich Day", an episode of the TV series 30 Rock. He guest-starred in a 2009 episode of Rules of Engagement as the father of the main character, Jeff.
Dennehy starred as Elizabeth Keen's grandfather on the NBC series The Blacklist since the third season until his death from sepsis. He is replaced by actor Ron Raines during the show's eighth season.
In 2015 Dennehy co-starred in the Amazon Studios pilot Cocked with Jason Lee, Dreama Walker, Diora Baird, and Sam Trammell.
Dennehy also narrated many television programs including the Canadian-Irish docudrama Death or Canada.