The house was built by Henry Fairbanks in 1915 on a design by prominent Washington architect Waddy Wood. President Wilson bought it in the last months of his second term as President as a gift to his wife, Edith Bolling Wilson. He presented her the deed in December 1920, although he had never seen the house. The former president and his wife moved into the home on Inauguration Day, which in 1921 was March 4 (not the current date of January 20). Wilson made several modifications to the house, including: a billiard room, "stacks" for his library of over 8,000 books, and a one-story brick garage.

It was from the balcony of the house that Wilson addressed a crowd on November 11, 1923, as his last public appearance. While the Wilsons had few guests, former British Prime Minister David Lloyd George and former French Prime Minister Georges Clemenceau did visit the ailing former president there. After Wilson's death in 1924, Edith Wilson lived there until her death on December 28, 1961. She hosted First Lady Jacqueline Kennedy for a brunch in the formal dining room. Edith bequeathed the property and all of its original furnishings to the National Trust for Historic Preservation.