Strictly speaking, Blair House refers to one of four existing structures that were merged to form a single building.

[6] The original brick house was built as a private home for Joseph Lovell, eighth surgeon general of the United States Army.

It was acquired in 1836 by Francis Preston Blair, a newspaper publisher and influential advisor to President Andrew Jackson, and remained in his family for the following century.

[2] The move was prompted in part by a request from Eleanor Roosevelt, who found the casual familiarity Winston Churchill displayed during his lengthy war-time stays at the White House sometimes an imposition.

[3] On one occasion, Churchill tried to enter Franklin Roosevelt's private apartments at 3:00 a.m. to wake the president for a conversation.

[11] On November 1, 1950, Puerto Rican nationalists Griselio Torresola and Oscar Collazo attempted to assassinate President Truman in Blair House.

[11] The assassination was foiled, in part by White House policeman Leslie Coffelt, who killed Torresola but was mortally wounded by him.

The Jackson Place properties were internally combined into a single building and then merged with Blair–Lee House by way of a connecting structure occupying the alleyway that had separated them.

[16] Notable guests who have stayed at the President's Guest House or the formerly separate Blair House include Queen Elizabeth II, Nikita Khrushchev, Vyacheslav Molotov, Emperor Akihito, Charles de Gaulle, Abubakar Tafawa Balewa, François Mitterrand, Vladimir Putin, Boris Yeltsin, Hosni Mubarak, Margaret Thatcher, Gloria Macapagal Arroyo, Javier Pérez de Cuéllar, Nambaryn Enkhbayar, Aung San Suu Kyi, Tony Blair, Narendra Modi, Lee Hsien Loong, Hamid Karzai, Benjamin Netanyahu, Luiz Inácio Lula da Silva, Justin Trudeau, Rishi Sunak and Anthony Albanese.

[21] In 1992, President-elect Bill Clinton chose to stay at the Hay–Adams Hotel instead of the guest house and, in 2009, a request by President-elect Barack Obama to take-up residence at the President's Guest House two weeks early was rejected because of its prior commitment to international dignitaries, include former Australian prime minister John Howard.

Its northern side along Jackson Place abuts Trowbridge House, a separate presidential residence.

The room is furnished with 18th-century English pieces, along with Chinese vases from the Ming and Qing (Kangxi reign) dynasties.

[33] The centerpiece of the Treaty Room in the former Peter Parker House is a 22-seat mahogany table that sits on an 1890 Sarouk rug.

A photographic portrait of Empress Dowager Cixi that was presented as a diplomatic gift to the United States by Qing Dynasty China in 1905 hangs in the room.

The Blair House Foundation, a private 501(c)(3) organization, finances the preservation of historic furnishings and art.

The board of trustees of the Blair House Foundation is chaired by Sarah Perot with Selwa Roosevelt serving as Chairman Emeritus.

[36] The house is operated by full-time staff who are non-residential but customarily live-in during periods of occupancy by a visiting dignitary.

[2] If two or more foreign visitors of equal rank are visiting Washington, neither is invited to stay at the President's Guest House to avoid the perception of favoritism.