Established in 1928 by action of the Board of Trustees to "make revolving exhibitions of contemporary arts and crafts available for visitation and study to students," the Howard University Gallery of Art was formally opened with a traveling exhibition of oil paintings, water colors, and drawings assembled and circulated by the College Art Association of America on April 7, 1930. After the success of this exhibition, a policy and program leading to the development of a permanent collection was adopted. James V. Herring, founder of the Department of Art, and James A. Porter, internationally renowned art historian and critic, were the earliest directors.

Henry O. Tanner's Return from the Crucifixion, an oil tempera painting, which is the last completed work of the artist, was one of the earliest acquisitions. This historic work is still a jewel of the collection.

Since the initial acquisition, numerous purchases and gifts from friends and faculty of the University, private collectors, art foundations, and various branches of the federal government have entered the permanent collection. The artifacts of Alain Locke, the esteemed philosopher, began the encyclopedia collection of African artifacts, while the Kress Foundation set up the collection of Renaissance and Baroque paintings. Other significant contributions and acquisitions, such as the Irving Gumbel collection of European prints from the 16th to the 19th centuries, and the array of paintings, sculptures, drawings, and prints by African American and other 20th century artists, have allowed the collection to grow exponentially.

The Gallery, serving as a study and research facility for the University and scholarly communities, offers rotating exhibitions of national and international artists, augmented with selections from the permanent collection in the galleries named for the first directors, and the eminent professors Lois Mailou Jones and James Lesesne Wells.