In 1942, Denning married 1940s horror film queen Evelyn Ankers (co-star of The Wolf Man, Ghost of Frankenstein and Son of Dracula), who retired from films at the age of 32 after they were married. He and Ankers had a daughter, Diana Denning (later Dwyer). After Ankers' death from cancer in 1985, Denning remarried, to Patricia Leffingwell. Denning and Ankers are buried at Maui Veterans Cemetery in Makawao, Hawaii.
On television, he starred as the title character in the 1950 syndicated adventure series Ding Howe and the Flying Tigers. He was cast as Dr. Greg Graham in the 1959 series, The Flying Doctor. He also starred as the title character in the detective series Michael Shayne (1960–1961) and shared title billing with Barbara Britton in the detective series Mr. and Mrs. North (1952–1954).
He appeared three times on the ABC religion anthology series Crossroads, as Dr. Ira Langston in "Chinese Checkers" (1955) and as the Reverend George Bolton in "The Bowery Bishop" and as the Reverend Lloyd E. Williams in "The Pure White Orchid" (both 1956). According to Denning, his military Service effectively disrupted his acting career, and after his discharge from military Service it would be another year and a half before Paramount Pictures offered Denning any more acting work. During that time period, Denning and his family lived in a mobile home that he alternately parked at Malibu and Palm Springs. His period of unemployment ended when he was hired to star on the radio opposite Lucille Ball in My Favorite Husband.
In other activity on old-time radio, Denning played Uncle Jack in It's a Crime, Mr. Collins (1956-1957) on the Mutual Broadcasting System. He also was the second actor to play Jerry North in the radio version of Mr. and Mrs. North.
Denning later appeared in several 'B' crime drama films before starring in a number of science fiction and horror films. In 1957, he began the first of what would become a steady series of television appearances, usually as a supporting character, though he did star briefly in two television dramas, The Flying Doctor (1959), and Michael Shayne (1960–61).
Denning has a star at 6932 Hollywood Boulevard in the Television section of the Hollywood Walk of Fame. It was dedicated on February 8, 1960.
In 1964-1965, Denning played Steve Scott in the comedy series Karen. In later life, he had a recurring role as the fictitious governor of Hawaii, Paul Jameson, in the CBS television crime drama series, Hawaii Five-O (1968–1980), starring Jack Lord.
In 1968, Denning completed his last film, a comedy titled I Sailed to Tahiti with an All-Girl Crew. Semi-retired and living on the island of Maui with his wife, Denning was contacted by Producer Leonard Freeman, who offered him the supporting role as the governor of Hawaii in the TV detective series, Hawaii Five-O. In order to persuade Denning to sign on in the recurring role, Freeman guaranteed Denning five-hour days and a four-day work week.
