He was born Ralph Rathgeber in Minneapolis, Minnesota, the son of Ralph and Magnhild Senovia Haavig Meeker Rathgeber. He made his film debut in 1951 with a small role in MGM's Teresa, followed by a starring role in the Swiss-made Four in a Jeep, directed by Leopold Lindtberg. In 1953 he was cast as a misfit ex-cavalryman in the classic western "The Naked Spur" directed by Anthony Mann.

For his performance in William Inge's Picnic, Meeker was awarded the New York Critic's Circle Award in 1954. Picnic became a classic film in 1955, with William Holden and Kim Novak starring in the roles originated by Meeker and Janice Rule. Around the same time, Meeker was cast in several low-budget films, including Code Two (1953), co-starring Keenan Wynn, in which Meeker portrayed a brash young rookie cop in Los Angeles.

Meeker starred as private detective Mike Hammer in the 1955 Robert Aldrich film of Mickey Spillane's Kiss Me Deadly. Many years later, this film acquired cult status and was seen as an influence on French New Wave directors such as Jean-Luc Godard. Meeker's portrayal of Hammer came to be lauded as one of the definitive "tough guy" performances. At the time, however, Meeker was unable to parlay the role into further starring film roles.

In 1957, he did co-star in Stanley Kubrick's Paths of Glory, playing one of the condemned soldiers. Later films included 1961's Ada with Dean Martin and the 1967 drama The St. Valentine's Day Massacre, in which he played gangster George "Bugs" Moran. He also appeared in 1967's hit The Dirty Dozen as Captain Kinder, a military psychologist who attempts to analyze the men. Meeker portrayed police officers in 1969's The Detective with Frank Sinatra and The Anderson Tapes (1970) with Sean Connery. He was producer of the movie My Boys Are Good Boys (1978).

On television, Meeker starred in 1955 in the premiere episode of Alfred Hitchcock Presents, "Revenge", with Vera Miles, as well as in three other episodes of the Hitchcock series. He starred in the 1958 episode "A Man Called Horse" of NBC's Wagon Train. In 1959 and 1960, Meeker starred as U.S. Army Sergeant Steve Dekker in the series "Not for Hire". In 1963, he appeared in "The Bull Roarer" on ABC's medical drama about psychiatry, Breaking Point starring Paul Richards. He guest-starred in the 1964 episode "Swing for the Moon" of ABC's Channing, set on a fictitious college campus and costarring Jason Evers and Henry Jones. In 1967, he appeared in ABC's military-western Custer, with Wayne Maunder in the title role. He made guest appearances on numerous other TV series, including Ironside, CHiPs, Toast of the Town, The Outer Limits and Studio One.

He was a graduate of the Leelanau School in Glen Arbor Township, Michigan, and a member of their Hall of Fame. Meeker married twice. His first wife was actress Salome Jens. The marriage lasted from 1964 to 1966. His second marriage was to Colleen Meeker. Major success continually eluded him. He died of a heart attack on August 5, 1988, in Woodland Hills, California.