Since its completion in 1815-1816, the Governor's Room has served as a museum and reception hall celebrating the civic history of New York and the nation. Originally comprised of the central chamber only, the two side chambers were added in 1832 (west) and 1848-1849 (east). The Governor's Room houses one of the most important collections of late-18th- to mid-19th-Century American portraiture, including paintings by John Trumbull; historic furnishings, including pieces by Charles Christian and Honoré Lannuier; and other notable artifacts, such as the desk George Washington used as president while presiding in New York from 1789 to 1790.

Many distinguished guests have visited the Governor's Room, including President James Monroe, President Andrew Jackson, the Marquis de Lafayette, Albert Einstein, and Dr. Martin Luther King Jr. The room hosted President-elect Abraham Lincoln in 1861, and served as the backdrop for his coffin in 1865 as he lay in state.