The Myer side of Joint Base Myer-Henderson Hall dates back to the Civil War. The land of the fort was originally owned by the grandson of Martha Washington, George Washington Parke Custis, which had come into public possession. Some of the land was designated as Fort Whipple, and in 1881, the fort was renamed Fort Myer, after General Albert J. Myer, surgeon and "Father of the Signal Corps".


In the late 1860's, the fort was designated as the nation's cavalry showplace, and used as the headquarters of the Signal Corps, because its high elevation made it great for visual communications. In the early 1900's, the fort was the site of the first military test flight. Orville Wright demonstrated the airplane for military observation at Myer in 1908. The plane successfully stayed in the air for one minute and eleven seconds. The second test flight lasted for four minutes before crashing, killing his passenger, Lieutenant Thomas Selfridge. Selfridge's death was the first powered-aviation fatality; Orville Wright survived with minor injuries.


During WWI, the fort served as a staging area for engineering, artillery, and chemical companies and regiments, while in WWII, the fort was a processing station for soldiers entering and leaving the Army. Also during that period, the Army's elite ceremonial units the U.S Army School of Music, the U.S Army Band, and the U.S Army Chorus relocated to the post in 1942. Presently, as an outcome of the 2005 BRAC, Fort Myer combined with the Marine Corps' Henderson Hall to become the first Joint Base in the Department of Defense, forming Joint Base Myer-Henderson Hall.