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Murray Hamilton first stepped on a Broadway stage in 1945; among his subsequent theatrical credits was the original production of Mister Roberts and his Tony-winning stint in 1964's Absence of a Cello. Hamilton's film career began with a minor role in Bright Victory (1951). He often played abrasive, cynical characters, such as the "feller sufferin' from R.O.T.C" in 1958's No Time for Sergeants, but he occasionally essayed good-guy roles, notably as James Stewart's foredoomed partner in The FBI Story (1959). Murray Hamilton is best known to many moviegoers for his role as the bombastic mayor in 1975's Jaws, a role which he won, according to the film's scenarist Carl Gottlieb, thanks to his acute ability "to portray weakness disguised as strength."

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