Artists represented in the permanent collection included Vito Acconci, Josef Albers, Robert Arneson, Jennifer Bartlett, Robert Brady, John Buck, Christopher Bucklow, Deborah Butterfield, Enrique Martinez Celaya, Enrique Chagoya, Dale Chihuly, John Coplans, Joseph Cornell, Gregory Crewdson, Robert Cumming, Stephen De Staebler, Richard DeVore, Jim Dine, Herbert Ferber, Llyn Foulkes, Judy Fox, Sam Francis, David Gilhooly, David Hockney, Diane Itter, Ferne Jacobs, Bill Jacobson, Jasper Johns, Donald Judd, Ron Kent, William Kentridge, Sanit Khewhok, Edward Kienholz and Nancy Reddin Kienholz, Sol LeWitt, Ken Little, Tony Marsh, Junko Mori, Yasumasa Morimura, Robert Motherwell, Vik Muniz, Jay Musler, Ron Nagle, Otto and Gertrud Natzler, Louise Nevelson, Catherine Opie, Dennis Oppenheim, Otto Piene, Kenneth Price, Lucie Rie, Liza Ryan, Alison Saar, Lucas Samaras, Adrian Saxe, James Seawright, Joseph Seigenthaler, Andres Serrano, David Smith, Kiki Smith, Rudolf Staffel, Pat Steir, Frank Stella, Jason Teraoka, Masami Teraoka, Mark Tobey, Richard Tuttle, Peter Voulkos, Kara Walker, Andy Warhol, William Wegman, Tom Wesselmann, Beatrice Wood, Cindy Wright and Daisy Youngblood.
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 Cooke's daughter, Alice Spalding, in 1968 and operated it as an annex for the display of Japanese prints from 1970 to 1978.
Following interior renovation and the construction of the Milton Cades Pavilion, the museum opened to the public in October 1988.
In addition to galleries, the museum consisted of a shop, cafe, administrative offices, storage and work areas, and a director residence.
The grounds display sculpture by Satoru Abe, Charles Arnoldi, Deborah Butterfield, Jedd Garet, George Rickey, Toshiko Takaezu, DeWain Valentine and Arnold Zimmerman, and a wall painting by Paul Morrison.