Descended from some prominent families in old New York City social circles, Wilmerding was educated at Harvard, receiving his A. B. in 1960, his masters in 1961, and his Ph.D. in 1965. From 1977 to 1983 he served as senior curator at the National Gallery of Art, in Washington, DC, and as its Deputy Director from 1983 to 1988. He currently serves as Christopher Binyon Sarofim Professor of American Art at Princeton.
At the May, 2004 opening of the National Gallery of Art's exhibit 'American Masters from Bingham to Eakins', Wilmerding generously announced that his entire collection would remain at the Gallery in perpetuity, including works by such well-known artists as Martin Johnson Heade, Fitz Henry Lane, John F. Peto, Joseph Decker, Winslow Homer, Thomas Eakins, Frederic Edwin Church, George Caleb Bingham, and John F. Kensett, and featuring certain of his favorite works by artists who visited and painted Maine's Mount Desert Island in Acadia National Park, where he has summered for many years. His contribution broadened and deepened the Gallery's holdings by adding many examples of types of works that the Gallery had not yet managed to acquire.
- American Marine Painting (Harry N. Abrams, 1987)
- American Views (Princeton University Press, 1991)
- The Artist's Mount Desert: American Painters on the Maine Coast (Princeton University Press, 1994)
- Compass and Clock (Harry N. Abrams, 1999)
- Signs of the Artist: Signatures and Self-Expression in American Painting (Yale University Press, 2003)
- "American Masters from Bingham to Eakins: The John Wilmerding Collection". National Gallery of Art. United States Government. Retrieved 17 January 2011.
- "Archived copy". Archived from the original on 2015-05-11. Retrieved 2015-04-26.
- "John Wilmerding's Profile". Dictionary of Art Historians.org. Retrieved 17 January 2011.
- Biography of John Wilmerding, National Gallery of Art.