The Museum design is French heritage. The style also permitted the inclusion of small niches in the museum tower for nesting birds.

Alice Tyler, widow of J. J. Audubon's great-grandson, Leonard Sanford Tyler, had been in contact with Susan Towles during the park's development. It was her wish that the large personal collection of Audubon material in her possession be placed on loan in the new Audubon Museum. Mrs. Tyler shipped her collection to Henderson in the spring of 1938 and the museum opened July 16, 1938.

The Tyler collection was later purchased in 1994 through numerous donations made to the Friends of Audubon, as well as contributions from the Preston Foundation and the Kentucky State Parks.

Today, the Museum proudly displays one of the world's largest collections of original Audubon art that made the wildlife artist a legend. But it is the personal artifacts and memorabilia that portray the often difficult life of Audubon - more starving artist than artistic success. The museum's four exhibit halls chronicle Audubon's life, including his 1810-1819 residence in Henderson, KY. Highlights of the collection include the American Bald Eagle oil, a four-volume edition of the Birds of America, a personal seal, handwritten journals, the silver service Audubon sent from England to his devoted wife, Lucy (replacing the service set that was lost during bankruptcy).