In 2013, the Pizzagalli Center for Art and Education was opened with two galleries, an auditorium, and a classroom, transforming the institution from seasonal (mid-May through October) to year-round operation.

[1] The core of the collection was formed by Electra Havemeyer Webb, a pioneering collector of American folk art who founded Shelburne Museum.

Mrs. Webb exchanged ideas with other major early collectors, including Katherine Prentis Murphy, Henry and Helen Flynnt and Henry Francis du Pont (who founded the Winterthur Museum and credited Mrs. Webb with inspiring him to collect American decorative arts).

These collections are increasingly relevant to regional audiences from varied backgrounds as the economic base of the community shifts away from farming and small-scale production.

American paintings include works by Bierstadt, Cassatt, Chase, Copley, Heade, Homer, Eastman Johnson, Lane, Grandma Moses, Peto and Andrew Wyeth.

A significant group of European paintings and pastels from the renowned Havemeyer collection includes works by Corot, Daubigny, Degas, Manet and Monet; they are exhibited in furnished rooms re-created from the Webbs' New York apartment, c. 1930, and are the only Impressionism pictures on public view in Vermont.

[6] Collections also include 225 horse-drawn vehicles (described as one of the best in the nation by Merri Ferrell, formerly curator of vehicles at the Long Island Museum of Art, History and Carriages);[7] 1,000 farming implements; and 5,000 hand tools that document woodworking, metalsmithing, coopering, weaving and spinning, leatherworking and woodcarving trades.

The collections are exhibited in a setting of 38 exhibition buildings, 25 of which were relocated to the museum; the 1871 Colchester Reef Light; three historic and three replica barns, including a 1901 Vermont round barn; a vintage operating carousel; blacksmith and wheelwright shops; a weaving shop with an operating Jacquard loom; a working exhibit of late 19th-century printing equipment; an 1840 one-room schoolhouse; an 1890 Vermont slate jail; an 1840 general store; a rare 18th-century up-and-down sawmill; a 19th-century covered bridge with two lanes and a footpath; the reconstructed office of noted Vermont physician D. C. Jarvis; an 1890 railroad station; a 1914 steam locomotive and 1890 private rail car; and the 1906 220-foot (67 m) steamboat Ticonderoga, which is a U.S. National Historic Landmark.

Webb believed that the sale violated the code of ethics of the American Alliance of Museums, which forbids the selling of artworks for purposes other than acquiring more art.