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In 1969, the Art Gallery of Ontario promoted her to Research Curator, and then to Curator of Canadian Art (the first such Gallery appointment) (1970–73). At the Gallery, she also served as the Acting Chief Curator (1972). From 1974 to 1999, Murray served as Director of the Robert McLaughlin Gallery in Oshawa where she organized over one hundred exhibitions and built a substantial collection, largely of Canadian art, as well as assisting with the creation of a new building by Arthur Erickson in 1987. From 2005-2006, Murray served as the Interim Executive Director and Chief Executive Officer of the McMichael Canadian Art Collection in Kleinburg, Ontario.

Murray was responsible for bringing the paintings of Tom Thomson to world attention through a series of exhibitions and books, including a biography. She has prepared a full-scale catalogue raisonné of his work, a project which took her over fifty years. She also has authored many books on the history of Canadian art, most notably Canadian Art in the Twentieth Century (1999), Northern Lights: Masterpieces of Tom Thomson and the Group of Seven (1994), and McMichael Canadian Art Collection: One Hundred Masterworks (2006). She has published over one hundred catalogues and two hundred articles on subjects ranging from folk art to contemporary artists.

Murray's collection of papers and over 600 interviews with artists can be found in Library and Archives Canada.