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Hackett debuted in 1959 with the role of Gail Prentiss in the television series, Young Doctor Malone. In 1961, she won a Theatre World Award, an Obie Award for Best Actress, and a Drama Desk Award for her Off-Broadway portrayal of Chris in Michael Shurtleff's play Call Me By My Rightful Name.
She had a recurring role in the CBS legal drama The Defenders (1961–1965) as the fiancée of Kenneth Preston (played by Robert Reed), partner in the father-and-son law firm led by patriarch Lawrence Preston (E.G. Marshall). She appeared regularly in scenes with both lead actors. She had a leading role in The Twilight Zone episode "A Piano in the House". In the 1963–1964 season, she guest-starred on Channing, an ABC drama about college life starring Jason Evers and Henry Jones.
Hackett had one of the starring roles in the 1966 Sidney Lumet film The Group, along with Candice Bergen, Larry Hagman, Richard Mulligan, Joanna Pettet, and others.
One of her notable film performances was the role of Catherine Allen, a young mother struggling to survive on the frontier, in the 1968 Western Will Penny, with Charlton Heston in the title role. Hackett also had notable parts in the classic Western comedy Support Your Local Sheriff!, with James Garner, and the 1973 murder mystery The Last of Sheila. After this, she primarily had parts in TV movies and on episodes of TV series.
She received top billing in the 1974 adaption of Michael Crichton's book The Terminal Man, where she played the brilliant Dr. Janet Ross, a psychiatrist who accurately predicts her patient's destructive behavior, opposite actors George Segal, Donald Moffat, and Richard Dysart.
In 1978, she appeared in a PBS adaptation of Mourning Becomes Electra as Christine Mannon. Her performance in that production earned her some of the best reviews of her career. Clive James said that it entitled her to be called a great actress. The same year, she was a regular in the cast of the short-lived CBS situation comedy Another Day, portraying Ginny Gardner.
She appeared in the September 22, 1979, episode "Grass Is Always Greener" of The Love Boat as Julie McCoy's former classmate from the line's cruise director course.
Hackett won the Golden Globe Award for Best Supporting Actress - Motion Picture and was nominated for the Academy Award for Best Supporting Actress for her performance in the 1981 film Only When I Laugh, the last film she made before her death. She could also be seen in Paul Simon's 1980 film One Trick Pony.