Aletter's Broadway debut came in 1950 as a replacement for Eli Wallach in Mister Roberts. During the 1950s, he appeared on Broadway in Bells Are Ringing, Time Limit, and Wish You Were Here.

He soon moved on to a prolific television career, appearing as a guest on numerous shows between 1956 and 1988. Aletter starred in three programs in the 1960s, beginning with Bringing Up Buddy, a CBS sitcom during the 1960–1961 season, featuring Aletter with Enid Markey and Doro Merande, who portrayed his overprotective spinster aunts to Aletter's character, Buddy Flower, a bachelor stockbroker. He appeared in the eighth episode of Lucille Ball's The Lucy Show in the 1962 segment, "Lucy The Music Lover." Aletter was cast as Dr. Sam Eastman, an ear-nose-throat specialist who adores classical music.

On April 20, 1958, Aletter married Lee Meriwether, Actress and former Miss America, in San Francisco, California. They divorced in 1974. They had two daughters, actresses Kyle Aletter-Oldham and Lesley Aletter. He married his second wife, Estella, former Miss Hurricane Hunter, in 1984; he had two stepdaughters, Julia and Alexandria Hodes.

Aletter's first wife, Lee Meriwether, a former Miss America, guest-starred once on Bringing Up Buddy. After Bringing Up Buddy, Aletter guest-starred in the ABC crime drama, Target: The Corruptors, the CBS anthology series, The Lloyd Bridges Show, and NBC's medical drama The Eleventh Hour. He portrayed murderer Harry Collins on the 1963 Perry Mason episode, "The Case of the Skeleton's Closet". Also in 1963, he co-starred in The Twilight Zone episode "The Parallel". In 1964, he played murder victim, television news reporter, Tommy Towne, in "The Case of the Arrogant Arsonist."

In the 1964–1965 season, Aletter appeared in The Cara Williams Show, with Cara Williams as his television wife. The two worked at the same company in violation of policy that employees could not marry each other and maintain their employment for that company. The show hence focused on how the couple kept the marriage secret.

In the 1965–1966 season, he guest-starred in two episodes of the ABC war drama, Twelve O'Clock High, once as Lt. Col. Bill Christy and also as a sergeant in public relations.

Aletter had another regular role in It's About Time, a Sherwood Schwartz series on CBS in 1966–1967.

He played Professor Irwin Hayden in the Richard Donner-directed, 36-part, live-action cliffhanger serial, Danger Island, on The Banana Splits Adventure Hour which aired on Saturday mornings on NBC from 1968 to 1970. In the fall of 1970, he had a supporting role in the NBC sitcom, Nancy.

Aletter also played George Snyder on the 1970s sitcom, Maude (which starred Bea Arthur), in the episode "Love And Marriage" (season one, episode seven).

On January 8, 1978, Aletter played advertising executive, Mr. Prescott, in the episode "The Commercial" of the CBS sitcom All in the Family.

Aletter worked with the Screen Actors Guild, having been elected as a vice President in 1987.

On May 13, 2009, Aletter died of cancer at the age of eighty-three at his home in Tarzana, California. He was survived by his second wife, two daughters, two stepdaughters, and a granddaughter.