Widmark was born in Sunrise Township, Minnesota, the son of Ethel Mae (née Barr) and Carl Henry Widmark. His father was of Swedish descent and his mother of English and Scottish ancestry. Widmark grew up in Princeton, Illinois, and also lived in Henry, Illinois for a short time, moving frequently because of his father’s work as a traveling salesman. He attended Lake Forest College, where he studied acting and also taught acting after he graduated. Widmark made his debut as a radio actor in 1938 on Aunt Jenny’s Real Life Stories. In 1941 and 1942, he was heard daily on the Mutual Broadcasting System in the title role of the daytime serial Front Page Farrell, introduced each afternoon as “the exciting, unforgettable radio drama… the story of a crack newspaperman and his wife, the story of David and Sally Farrell.” Farrell was a top reporter for the Brooklyn Eagle. When the series moved to NBC, Widmark turned the role over to Carleton G. Young and Staats Cotsworth. During the 1940s, Widmark was also heard on such network radio programs as Gang Busters, Inner Sanctum Mysteries, Joyce Jordan, M.D., Molle Mystery Theater, Suspense and Ethel and Albert. In 1952 he portrayed Cincinnatus Shryock in an episode of Cavalcade of America titled “Adventure on the Kentucky.” He returned to radio drama decades later, performing on CBS Radio Mystery Theater (1974–82), and was also one of the five hosts on Sears Radio Theater (as the Friday “adventure night” host) from 1979–81. Widmark appeared on Broadway in 1943 in F. Hugh Herbert’s Kiss and Tell. He was unable to join the military during World War II because of a perforated eardrum. He was in Chicago appearing in a stage production of Dream Girl with June Havoc when 20th Century Fox signed him to a seven-year contract.

Widmark’s first movie appearance was in Kiss of Death (1947), as the giggling, sociopathic villain Tommy Udo. His most notorious scene found Udo pushing a wheelchair-bound woman (played by Mildred Dunnock) down a flight of stairs to her death. Widmark was almost not cast. He said, “The director, Henry Hathaway, didn’t want me. I have a high forehead; he thought I looked too intellectual.” Hathaway was overruled by studio boss Darryl F. Zanuck. “Hathaway gave me kind of a bad time,” recalled Widmark. Kiss of Death was a commercial and critical success: Widmark won the Golden Globe Award for New Star Of The Year – Actor, and was nominated for the Academy Award for Best Supporting Actor for his performance. Widmark played “Dude” in the Western film Yellow Sky (1948), with Gregory Peck and Anne Baxter. His name was billed third, above the title. Widmark then co-starred with Gene Tierney and Googie Withers in Jules Dassin’s Night and the City and with Paul Douglas, Barbara Bel Geddes, Jack Palance and Zero Mostel in Elia Kazan’s Panic in the Streets (both 1950). They are considered classic examples of film noir. Around the same time, Widmark starred with Sidney Poitier in the gripping racial melodrama No Way Out (also 1950). In 1952, Widmark had his handprints cast in cement at Grauman’s Chinese Theatre. During his stint at Fox, he appeared in The Street with No Name (1948), Don’t Bother to Knock (1952) with Marilyn Monroe, and Samuel Fuller’s Pickup on South Street (1953). Widmark appeared in two Fox westerns: Garden of Evil opposite Gary Cooper, and Broken Lance (both 1954) with Spencer Tracy. He also appeared in Vincente Minnelli’s film The Cobweb (1955) with Lauren Bacall.

Widmark starred in, and also produced, a naval drama set during the Cold War, The Bedford Incident (1965), modelled loosely on the Herman Melville novel, “Moby Dick”. He is also credited with producing his films Time Limit (1957) and The Secret Ways (1961). Other films in this period were The Alamo (1960) with John Wayne as Davy Crockett and Widmark as Jim Bowie, Judgment at Nuremberg (1961), How the West Was Won (1962), John Ford’s Two Rode Together (1961) and Cheyenne Autumn (1964) and, in “Madigan” (1968), as a police detective in the title role, which he later reprised in a televion series of the same name. During the 1970s, Widmark’s films included Murder on the Orient Express (1974), Michael Crichton’s Coma (1978), and The Swarm (1978). In all, Widmark appeared in over 60 films before making his final movie appearance in True Colors (1991). Widmark was a guest on What’s My Line? in 1954. The following year, he made a rare foray into comedy on I Love Lucy, portraying himself when a starstruck Lucy trespasses onto his property to steal a souvenir. Widmark finds Lucy sprawled out on his living room floor underneath a bearskin rug. Returning to television in the early 1970s, Widmark received an Emmy nomination for his performance as Paul Roudebush, the President of the United States, in the TV movie Vanished! (1971), a Fletcher Knebel political thriller. In 1972–73, he reprised his detective role from Don Siegel’s Madigan (1968) with six 90-minute episodes on the NBC Wednesday Mystery Movie. The next year, he participated in a mini-series about Benjamin Franklin, transmitted in 1974, which was a unique experiment of four 90-minute dramas, each with a different actor impersonating Franklin: Widmark, Beau Bridges, Eddie Albert, Melvyn Douglas, and, portraying Franklin at age twelve, Willie Aames. The series won a Peabody Award and five Emmys. During the 1980s, Widmark returned to TV with a half-dozen TV movies.

Widmark was married to playwright Jean Hazlewood from 1942 until her death in 1997. They had a daughter, Anne Heath Widmark, an artist and author who was married to baseball player Sandy Koufax from 1969 to 1982. In 1999, Widmark married Susan Blanchard, the daughter of Dorothy Hammerstein and stepdaughter of Oscar Hammerstein II; she had been Henry Fonda’s third wife. Green City, Missouri, is the site of Widmark Airport (FAA LID: MO83) in northeastern Missouri. Towns the size of Green City, whose population numbered only 688 inhabitants in 2000, usually do not have airports, but Widmark owned a cattle ranch in the area during the 1950s and 1960s. Widmark contributed funds to the construction of an airport which led to its being named in his honor. Having retired in 2001, Widmark died, after a long illness, on March 24, 2008, at his home in Roxbury, Connecticut at the age of 93. Widmark’s illness had been aggravated by a fall he had suffered during the previous year. At the 2009 Academy Awards, Richard Widmark was honored in the Memorial Tribute. His interment was at Roxbury’s cemetery.