In 1985 the Office of the Assistant Secretary for Museums was created to replace the Assistant Secretary for Museum Programs. In addition to duties performed by the predecessor office, the Assistant Secretary for Museums oversaw the administration of all the Smithsonian museums. During this time the office collaborated with the Assistant Secretary for Research in oversight of scholarly and presentational activities in the science museums.

In 1992 the Office was renamed the Office of the Assistant Secretary for the Arts and Humanities as part of a reorganization of Smithsonian Institution administration. At this time the administration created a more defined line between science museums and arts and humanities museums, the latter being the responsibility of the new Assistant Secretary for the Arts and Humanities. The incumbent in both offices advised the Secretary and Under Secretary on issues relating to museum policies, operations, and advocacy, especially as they related to accessibility, exhibitions, and museum education. In 1994 the office was again renamed the Assistant Provost for the Arts and Humanities, reporting to the Office of the Provost. The office was abolished in a 1995 managerial change.

Tom L. Freudenheim served as Assistant Secretary for Museums, 1985-1991; Assistant Secretary for the Arts and Humanities, 1992-1994, and Assistant Provost for the Arts and Humanities, 1995.