The President's House, located northeast of the Wren Building and facing the Brafferton, was built in 1732 and has been used by every William & Mary president. It is the oldest university president's house in the United States.

In 1781, during the American Revolution, the President's House served as Cornwallis's headquarters. It accidentally burned while occupied by French troops before the Battle of Yorktown and was rebuilt with money from French king Louis XVI. In 1862, during the Civil War, the house was used for various purposes including as Federal Headquarters for the area. After a raid by Confederate General Mosby's men on Union troops in Williamsburg, defensive works were thrown up by the Federal troops across the Old Campus in the spring 1865. The President's House was used in these works and some of its windows and doors were bricked up and loopholed.

The house has undergone a number of renovations in its history. From 1928-1931, the President's House, along with the Brafferton and the Wren Building, were restored to their colonial appearance as part of John D. Rockefeller, Jr.'s restoration of Williamsburg. The kitchen building was reconstructed for use as the President's study and library. The garage built by President Benjamin Ewell remained as a fire house. A new small, frame building was built near the kitchen for storing tools and fire apparatus.