The museum features Classical, Medieval, Renaissance, Baroque, Celtic, and Asian art and artifacts in three distinct galleries totaling 2,700 square feet (250 m2) of space.

[5] The museum is located on the renovated lower level of Bellarmine Hall which was designed in 1921 in the English manorial style.

Formerly known as Hearthstone Hall because of its many fireplaces and chimneys, this forty-four room mansion was built by Walter B. Lashar, owner of the American Chain and Cable Company.

The Meditz Gallery, which resembles an early Christian basilica in plan, showcases ten paintings from the Italian Renaissance and Baroque periods, works gifted to the University by the Samuel H. Kress Foundation through Bridgeport's Discovery Museum.

In 2017, the Fairfield University Art Museum received a transformative gift of over 1200 prints from the artist, collector, and master printer James Reed.