The Bank's headquarters has had three locations in downtown Richmond, starting in offices near the federal courts in 1914. A headquarters building was constructed on the city's historic Capitol Square and the Bank offices were moved there in 1922. The current headquarters building, overlooking the James River, opened in 1978. The Richmond Fed has had offices in Baltimore since 1918 and in Charlotte, N.C., since 1927. The Bank formerly had operations in Charleston, W.Va.; Columbia, S.C.; and Culpeper, Va.

Since its founding, the Richmond Fed has had seven chief executives, starting with George Seay, who led the effort to bring the Bank to Richmond and served as governor from 1914 until 1936. Following Seay, the presidents of the Richmond Fed were Hugh Leach, Edward A. Wayne, Aubrey N. Heflin, Robert P. Black and J. Alfred Broaddus Jr. The Bank's current president is Jeffrey M. Lacker, who was appointed in 2004.