Virginia House was completed in 1928, and in 1929 it was presented to the Virginia Historical Society with the Weddells retaining lifetime tenancy. Virginia House became the sole responsibility of the Virginia Historical Society in 1948 after Ambassador and Mrs. Weddell, and Mrs. Weddell's personal maid Violet Andrews, were killed in a train crash on New Year's Day.

Today Virginia House is owned and operated by the Virginia Historical Society. The house is open for tours during the week and on weekends. It is also available for meetings and special events. The Gallery in the Sulgrave wing has a rotating schedule of exhibits.