In 1957, Rust was chosen as a replacement in Eugene O'Neill's Long Day's Journey Into Night, with Frederic March (1897-1975) and Florence Eldridge, March's wife. The play was performed in the prestigious Helen Hayes Theatre.
In 1958, Rust signed a contract with Columbia Pictures, along with other young Hollywood aspirants Michael Callan and Yvonne Craig. He appeared in 1959 in The Legend of Tom Dooley, a Western film starring Michael Landon, unrelated to the popular song "Tom Dooley" released the previous year by The Kingston Trio. Rust also appeared in 1960 in the crime drama This Rebel Breed about rival narcotics gangs in high schools.
He starred in 1960 as Dobie with Randolph Scott in the western film Comanche Station. His films in 1961 included Homicidal, a thriller starring Glenn Corbett, and Underworld USA, a study of revenge starring Cliff Robertson. He starred as Oliver in the 1962 film Walk on the Wild Side with Laurence Harvey. During this period, Rust also appeared in several western television programs, including The Brothers Brannagan with Stephen Dunne and Mark Roberts, The Rifleman starring Chuck Connors, Tales of Wells Fargo starring Dale Robertson, Sugarfoot with Will Hutchins, Bronco with Ty Hardin and Have Gun Will Travel with Richard Boone. He twice guest starred on ABC's 77 Sunset Strip with Efrem Zimbalist, Jr. He also appeared in 1961 on James Franciscus's CBS series The Investigators.
In 1962, he won the role of the 24-year-old attorney Hank Tabor on Sam Benedict, with Edmond O'Brien in the starring role, over some sixty competitors because of his acting experience and his educational background. The series, however, facing competition from new variety programs launched by Roy Rogers and Dale Evans on ABC and Jackie Gleason on CBS, lasted for only twenty-eight episodes.
After Sam Benedict, Rust appeared in various television programs, including Gary Lockwood's The Lieutenant, which occupied the former time slot on Saturday nights held the previous year by Sam Benedict. He guest starred on Perry Mason with Raymond Burr, Bonanza, Christopher George's The Rat Patrol, and Cade's County with Glenn Ford. In 1969, he appeared in a Roger Corman biker cult film titled Naked Angels. His last named role was in 1990 as Sheriff Blanchfield in the film Double Revenge about a bystander who goes on a rampage against a bank robber.
Rust was divorced from the former Dionne Van Hessen. The couple had three children, Dorinda, Rachel, and Richard. Rust had a multitude of hobbies, including readings about religion and mysticism, oil paintings, sailing, music, and water skiing. Rust died at the age of fifty-six in Los Angeles, California, of a myocardial infarction.