While the Museum only dates to 1983, the university art collection has been in existence since its first gift – a portrait of the physicist Robert Boyle – in 1732.

[1] Throughout the years, gifts of art continued to accumulate including a donation of White Flower by Georgia O'Keeffe given to William & Mary in 1938 by Abby Aldrich Rockefeller.

This major work in the collection had indiscriminately "decorated" various campus walls, old and new, until it was re-discovered by President Thomas Ashley Graves Jr. in the 1970s.

In 1987, the second director, Mark Johnson oversaw the expansion of the facility and the first American Alliance of Museums accreditation in 1988.

Of particular note are Colonial American and English seventeenth and eighteenth century portraits; a survey collection of original prints and drawings from the fifteenth through the twenty-first centuries including Japanese prints and a major collection of German Expressionist works by Hans Grohs; and the Jean Outland Chrysler collection of American modern works interpreted in oils, drawings, watercolors, and sculpture.