The building itself represents three distinct architectural stages: the original 1904 classical revival mansion designed by Abram Garfield, the son of president James A. Garfield,[2] which has housed the museum since its opening in 1952, a brutalist addition built in 1975, and a 2005 addition designed by Randall Stout which now serves as the entrance to the museum.

The centerpiece of the Benwood Foundation's gifts to the community of Chattanooga is the Hunter Museum of American Art, originally known as the Ross Faxon House.

"The Hunter Museum portion of the project included a $22 million expansion and renovation, designed by Randall Stout that was completed in 2005.

[6] "The collection spans from the colonial period to present day and covers a wide variety of media including painting, sculpture, contemporary studio glass, and crafts.

"[8] In June 2015, the Hunter Museum of Art announced on its website that it had chosen a new executive director, Virginia Ann Sharber.