The structure that houses The Contemporary Museum was built as a residence in 1925 by Mrs. Charles Montague Cooke. At the same time, The Honolulu Academy of Arts was being built on the site of her former home on Beretania Street. The Makiki Heights home was designed by Hart Wood and later enlarged by the firm of Bertram Goodhue and Associates. The Honolulu Academy of Arts acquired the estate as a bequest from Mrs. Cooke's daughter, Alice Spalding, in 1968 and operated it as an annex from 1970 to 1978.

After passing through the hands of a private developer in the late 1970s, the property was acquired by a subsidiary of The Honolulu Advertiser. In 1986 the Twigg-Smith family offered it as a site for The Contemporary Museum. Following interior renovation by The CJS Group Architects and the construction of the Milton Cades Pavilion, the museum opened to the public in October 1988. In addition to the galleries, the museum now consists of The Museum Shop, The Contemporary Cafe, administrative offices, storage and work areas, and a residence for the director.