While Henry Huntington envisioned a collection of American art as early as 1919, his vision was not realized until 60 years later. In 1979 the Virginia Steele Scott Foundation made a major gift to The Huntington in memory of Virginia Steele Scott, art collector, patron, and philanthropist, which included a group of 50 American paintings, funds to construct a gallery to display the collection, and an endowment for its professional management.

Designed by Paul Gray, The Virginia Steele Scott Galleries of American Art opened to the public in 1984, inaugurating American art as a significant part of The Huntington's collections. Since then, the American art collection has grown dramatically, largely through the support of the Scott Foundation, the Huntington’s Art Collectors' Council, generous donations to the collection, and significant long-term loans.

Utilizing more than 21,500 square feet, the Scott Galleries are one of the largest presentations in California of American art from the colonial period through the mid- 20th century. The Huntington's American art holdings now number about 245 paintings, 60 works of sculpture, 990 decorative art objects, 8,500 prints and drawings, and 1,800 photographs.

Frederick Fisher’s modern classical wing, the Lois and Robert F. Erburu Gallery, joined the neoclassical Scott Galleries in 2005. Together, the galleries sit beautifully in the Huntington landscape, inviting views of the mountains and gardens from the glass loggia and helping to develop a sense of interplay between the works of art inside and the gardens outside.

In 2016, the Scott Galleries underwent an 8,600 square-foot expansion including 5,000 square feet of gallery space with dramatic, colorful displays that showcase early American paintings, furniture, and works of decorative art, and offer important insights into the history of American art practice.

The inaugural exhibition, “Becoming American: Highlights from the Jonathan and Karin Fielding Collection,” showcases more than 200 works from the Fieldings’ collection of 18th- and early 19th-century American art works, including paintings, sculpture, furniture, ceramics, metal, needlework, and other related decorative arts. Some of the objects are promised gifts to The Huntington. In its rich diversity, the Fielding Collection offers a rare opportunity to explore early American history through objects made for daily use and through images of the people who used them. highlights recent acquisitions and long-term loans from public and private collections including paintings by John Singleton Copley, Frederic Edwin Church, Mary Cassatt, John Singer Sargent, John Sloan, Robert Motherwell, and Sam Francis, as well as American decorative arts ranging from silver by Paul Revere to furniture designed by Frank Lloyd Wright. An important part of the permanent installation is a gallery devoted to the work of early 20th-century Pasadena architects Charles and Henry Greene.

The galleries include a space for temporary exhibitions. The Susan and Stephen Chandler Wing showcases focused exhibitions from The Huntington’s rich collection of American prints, drawings, and photographs.