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Telfair Museums’ collection was formally founded with the bequest of Mary Telfair in 1875. The bequest included the house and many of its contents, including Mary’s collection of paintings (family portraits and paintings acquired on travels to Europe), two sculptures (relief plaques with portraits of Mary and her sister Margaret), and Telfair furniture belonging to various family members between the late 18th century through the 1870s. It is important to note that, apart from these items, the Telfair family did not own or bequeath a significant collection of art to establish the museum.

The museum’s initial fine art collection was formed by the first director, Carl Brandt. Brandt, a well-known artist, traveled to Europe and purchased or commissioned the first works for the collection, including the sculptures outside of the Telfair Academy, the plaster casts in the sculpture gallery and paintings by European academic artists such as Cesare Laurenti and Julian Story. After Brandt’s death in 1905, the collection was further developed by Gari Melchers, who served as the museum’s fine art advisor from 1906 until 1916, and unofficially through the 1920s. It was under Gari Melchers that the museum acquired some of its most admired works by American Impressionist and Ashcan School artists, including George Bellows’ Snow-Capped River, Childe Hassam’s Brooklyn Bridge in Winter, and Robert Henri’s La Madrileñita.

The Owens-Thomas House bequest in 1951 added considerably to the museum’s decorative arts collection. In addition to the gift of the house, the donation included a significant number of decorative arts objects composed primarily of Owens family furnishings, along with American and European pieces dating from the late 18th century to the early 20th century.

The museum’s collecting efforts slowed considerably after the Gari Melchers era. As a result, the museum’s collection is weak in most of the major art movements of the 20th century, such as Cubism, Abstract-Expressionism, and Pop Art. The Museum’s collecting efforts began again in earnest when the idea of the Jepson Center for the Arts was formed in the 1990s, with attention focused on assembling modern and contemporary works appropriate for display in the new building. A cornerstone of the museum’s contemporary holdings is the Kirk Varnedoe Collection, donated on the occasion of the Jepson Center’s opening, which features works on paper by some of the most pivotal artists of the past fifty years.

The scope of the Telfair’s collection today primarily encompasses American and European art from the 19th century to the present, in a broad range of media. There are currently over 7,000 works of art in the collection, divided roughly equally between fine and decorative arts. The museum’s three architecturally-significant buildings are also considered part of its permanent collection.