In 1950 he won a scholarship to a New York drama school.

George Seaton was in New York casting his 1956 film The Proud and Profane and gave Stricklyn a one-scene role. He then moved to Los Angeles to further his film career. Stricklyn also appeared in the role of Tim Hansen in the 1958 film "The Return of Dracula." After his performance in Ten North Frederick (1958), he was given a contract with 20th Century-Fox, but it wasn't renewed following The Remarkable Mr. Pennypacker (1959). His first lead role was as Jesse James in Young Jesse James (1960), and he also had roles in The Big Fisherman (1959), The Lost World (1960), The Plunderers (1960), Arizona Raiders (1965), Track of Thunder (1967) and Dogpound Shuffle (1975). However, in later years he received fewer film roles and he returned to theatre work.

In 1965 Stricklyn was introduced to a furniture refurbisher David Galligan and they became lifetime companions. Galligan later became a noted stage Director.

Stricklyn took work in a fudge factory and then worked as a typist for a mailing company. In 1973 he joined the public relations firm John Springer Associates in Los Angeles and became one of the most influential publicists in Hollywood, working with some of the biggest names in entertainment, including Henry Fonda, Shelley Winters, Janet Leigh, Elizabeth Taylor, and Bette Davis. He also handled the US debut of the Rubik's Cube. He eventually became the head of the company's West Coast office.

In 1983 Stricklyn and Charlotte Chandler wrote a one-hour one-man show, Confessions of a Nightingale, about Tennessee Williams. Stricklyn portrayed Williams in the production, which was adapted from Chandler's interviews with Williams. Critic John Simon wrote in New York magazine: "Ray Stricklyn ... does a fine job as Williams. The accent may waver a bit, but all those small mannerisms, tics, idiosyncratic intonations, hesitancies, shifts of mood are fraught with authenticity."

Stricklyn had the role of Howard Alston Hawkins in Days of Our Lives (1991-1992). He made two guest appearances on the CBS courtroom drama series Perry Mason. In 1960 he played defendant Gerald Norton in "The Case of the Bashful Burro," and in 1963 he played Reed Brent in "The Case of the Festive Felon."

After falling ill with emphysema in 1997, he began writing his coming out autobiography. Published in 1999, Angels & Demons: One Actor's Hollywood Journey, published in Los Angeles by Belle Publishing, 297 pages, ISBN 0-9649635-4-X (hardback), is a candid and witty account of a man who, Stricklyn wrote, "might qualify as one who has had his 15 minutes in the limelight; perhaps even 20."

Ray Stricklyn: Actor whose boyish looks became a hindrance Obituary by Tom Vallance in The Independent, 29th. May, 2002, page 18. "Stricklyn stated that two factors had contributed to his lack of progress. First, his homosexuality (though he had well-publicised relationships with Joan Collins and Bette Davis) and secondly, his persistently youthful appearance."