According to the Vermont Encyclopedia, the museum is a cultural center for the community and "attracts a diverse audience from UVM, area colleges, and the general public.

Among the museum's initial collections were "fossils, stuffed birds, a sperm whale tooth, and a cannon ball that a local resident found while gardening.

[2] The formation of the modern Fleming Museum of Art came in 1929, when Katherine Wolcott, the niece and only heir of Robert Hull Fleming and an artist herself, traveled from Chicago to Burlington, intending to establish a scholarship in honor of her late uncle, who had graduated from the University of Vermont in 1862 before becoming a wealthy Chicago grain merchant.

The Fleming Museum building is an example of Colonial Revival architecture, with red bricks and boarding wood trim bordered white.

[2] The Marble Court was the museum's original entrance, and includes a two-story central courtyard with columns supporting a balcony on the second floor.

William Mitchell Kendall had built a similar space for the Cohen Memorial Fine Arts Building at George Peabody College for Teachers in Nashville, Tennessee.

New additions included a climate control system, corridor display cases, a new reception area, a museum store, and an altered gallery floor plan that allowed for exhibition space to be more flexible.