Dewhurst was born in Montreal, Quebec, the only child of Ferdinand Augustus “Fred” Dewhurst, owner of a chain of confectionery stores, and his wife, Frances Marie (née Woods) Dewhurst, a homemaker, whose father had been a “well-known athlete in Canada, where he had played football with the Ottawa Rough Riders”. The family naturalized as U.S. citizens before 1940. Colleen’s mother was a Christian Scientist, which faith Colleen would also embrace.  The Dewhursts moved to Massachusetts in 1928 or 1929, staying in Boston, Dorchester, Auburndale, and West Newton. Later they moved to New York City, and then to Whitefish Bay, Wisconsin. She attended Whitefish Bay High School for her first two years of high school, moved to Shorewood High School for her junior year, and finally graduated from Riverside High School in Milwaukee in 1942. It was around this time that her parents separated. Dewhurst went on to attend Milwaukee-Downer College for two years before moving to New York City to pursue an acting career.  One of Dewhurst’s most significant stage roles was in the 1974 Broadway revival of O’Neill’s A Moon for the Misbegotten as Josie Hogan, for which she won a Tony Award. She previously won the Tony Award for Best Featured Actress in 1961 for All the Way Home. She later played Katharina in a 1956 production of Taming of the Shrew for Joseph Papp.   She played Shakespeare’s Cleopatra and Lady Macbeth for Papp and, years later, Gertrude in a production of Hamlet at the Delacorte Theatre in Central Park. Dewhurst and George C. Scott met while working together in 1958, in Children of Darkness, while they were both married to other people.  She appeared in Alfred Hitchcock Mystery Hour in Night Fever in 1965 and with Ingrid Bergman in More Stately Mansions on Broadway in 1967. José Quintero directed her in O’Neill’s Long Day’s Journey into Night and Mourning Becomes Electra. She appeared in Edward Albee’s adaptation of Carson McCullers’ Ballad of the Sad Cafe, and as Martha in a Broadway revival of Who’s Afraid of Virginia Woolf, opposite Ben Gazzara which Albee directed.

She appeared in 1962 as Joanne Novak in the episode “I Don’t Belong in a White-Painted House” in NBC’s medical drama, The Eleventh Hour, starring Wendell Corey and Jack Ging.[5] Dewhurst appeared opposite her then-husband, Scott, in a 1971 television adaptation of Arthur Miller’s The Price, on Hallmark Hall of Fame, an anthology series, and there is another television recording of them together when she played Elizabeth Proctor to his unfaithful John in Miller’s The Crucible (with Tuesday Weld. In 1977, Woody Allen cast her in his film Annie Hall as Annie’s mother.  In 1972 she played a madam, Mrs. Kate Collingwood, in The Cowboys (1972), which starred John Wayne. In 1985, she played the role of Marilla Cuthbert in Kevin Sullivan’s adaptation of Lucy Maud Montgomery’s novel Anne of Green Gables, and reprised the role in 1987’s Anne of Avonlea (also known as Anne of Green Gables: The Sequel), and in several episodes of Kevin Sullivan’s Road to Avonlea. Dewhurst died before the character of Marilla could be written out and her final scenes were picked up off the editing-room floor and pieced together for her death scene. During 1989 and 1990, she appeared in a supporting role on the television series Murphy Brown playing the feisty mother of Candice Bergen’s title character; this role earned her two Emmy Awards, the second being awarded posthumously. Dewhurst won a total of two Tony Awards and four Emmy Awards for her stage and television work.  She was president of the Actors’ Equity Association from 1985 until her death from cervical cancer in 1991.