Erected in 1959, the present building was designed by architects Warren, Knight & Davis, and a major renovation and expansion by Edward Larrabee Barnes of New York was completed in 1993.

Among the earliest works to enter the collection were paintings by significant Alabama artists including the miniaturist Hannah Elliott and the landscapist Carrie Hill.

The collection features painting, sculpture, video, photography, works on paper, and installation art that illuminates movements and trends from the 1960s to the present, ranging from artists such as Joan Mitchell, Andy Warhol, Bill Viola, Lynda Benglis, Cham Hendon, Kerry James Marshall, Callum Innes, Grace Hartigan, Larry Rivers, Louise Nevelson, Frank Fleming and Philip Guston, to a generation of artists that are defining the new century.

The Modern and Contemporary Art collection also contains work by photographers William Christenberry, Robert Frank, Duane Michals, Gordon Parks, and Philip Trager, as well as images from the civil rights era by Danny Lyon, Spider Martin, Chris McNair, Charles Moore, and Wayne Sides.

[3] Since 2009, a permanent display of folk art has featured works by Bill Traylor, Thornton Dial, Alabama's outstanding quilters, and other self-taught artists.

One of the foundations of the museum's permanent collection, the European decorative arts comprise more than 12,000 objects including ceramics, glass, and furniture dating from the Renaissance to present day.

Cultures of ancient Costa Rica, Guatemala, and Panama are well represented: works include gold jewelry, metates, censors, volcanic stone figure sculpture, and ceramics.

Northern Andean objects include Sican ceremonial gold vessels and tumi, ceramics from the Moche, Chimu, Chancay, and Vicus cultures, Incan keros and mummy masks, and Peruvian textiles.

In April 1951 the newly established Birmingham Museum of Art presented a public "Opening Exhibition" housed in five unused rooms in City Hall.

The exhibition included some pieces from the existing Art Club collection as well as a large number of loaned works from museums across the Eastern half of the United States.

In the following years, the Kress Foundation made two important gifts to the museum: the trusteeship of a collection of Renaissance furniture and decorative objects in 1959, and the deed to the Italian paintings already on loan, along with eight additional works from the same period.

Further reworking of the east wing added a conservation lab, loading dock, and a second public entrance to the building in 1979, and the following year, gallery space was expanded by 28,000 square feet (2,600 m2).