Donahue was studying journalism at Columbia University and pursuing an acting career in stock productions when he landed his first film role, a bit part in "Man Afraid" (1957). Later that year, he supported Rock Hudson, Dorothy Malone and Robert Stack in "The Tarnished Angels". Despite such foolishness as the low-budget "Monster on the Campus" (1958) and several other small roles in teen-oriented fare, Warner Bros. signed Donahue to a multi-year contract in 1959. His first film for the studio, the sudsy "A Summer Place", cast him as the son of booze-soaked Dorothy McGuire and Arthur Kennedy and boyfriend of the then-Number One female teen star, Sandra Dee. Their pairing was a popular one and briefly put Donahue on equal footing with Elvis Presley and Pat Boone as a teen idol. Warner Bros., eager to capitalize on Donahue's ability to sell tickets at drive-in theatres, cast the actor in such typical efforts as "Palm Springs Weekend" (1963), a predictable romp stocked with the popular faces of the moment.
When his contract with Warner Bros. ended, Donahue was cast by Raoul Walsh in "A Distant Trumpet" (1964) as a fighting cowboy matched with Suzanne Pleshette, to whom he was briefly married. As the teen audience matured and tastes changed, Donahue found himself starring in such forgettable efforts as the murder mystery "Come Spy With Me" (1967). He had not worked in films for three years when Francis Ford Coppola hired him for "The Godfather, Part II". After the film's release there were a lot of "Wasn't that Troy Donahue?" remarks on TV talk shows and in the press, and columnists seemed to be wishing him well, but perhaps soured on Hollywood "promises," Donahue plunged into low-budget films with gay abandon. Some, such as "Cockfighter" (1975), had an artistic, interesting bent, but most were on the order of "Deadly Prey" (1987), "Sexpot" (1988), and "Attack of the Party Nerds" (1989). He did make cameos, along with other teen favorites of the 50s and 60s, in such films as "Back to the Beach" (1987), and John Waters' "Cry Baby" (1990), but Donahue seemed to disappear from mainstream fare. He could be seen in the 90s signing autographs at $10 per 8x10 glossy at Hollywood memorabilia collector shows alongside many other faces used and discarded by Hollywood.