Although Art Center held exhibitions since the early 1930s, it was not until 1985 when a formal department was established with a full-time director, Stephen Nowlin, a 1978 graduate of Art Center's Fine Art/Painting department, who is the VIce-President and Director of the Alyce de Roulet Williamson Gallery.

At the Pasadena Hillside campus, most exhibitions were displayed in Room 216, which was shared with Transportation Design. In 1991, in need of more permanent exhibition space, the Alyce de Roulet Williamson Gallery was designed and constructed in the space that was previously an outdoor atrium. The Williamson gallery opened in 1992 with an exhibition of works by Christopher Le Brun.

As of 2015, Art Center maintains six gallery spaces: the Alyce de Roulet Williamson Gallery, main student gallery, undergraduate Fine Art galleries, the Public Programs gallery, Hutto-Patterson Exhibition Hall (in the 870 building), and the Wind Tunnel Gallery.

Various staff and faculty work on the different exhibition spaces, but below are the full-time staff working with exhibitions:
Midge Quenell, Gallery Coordinator, 1970s - early 1980s
Stephen Nowlin, Vice-President, Director Alyce de Roulet Williamson Gallery, 1978 - present
Julian Goldwhite, Associate Curator, late 1980s - present