Today’s White House Military Office is actually an amalgamation of several previously independent offices and agencies.

Military representation in the White House originated with General Washington's Aide-de-Camp, whose role as Personal Aide to the President has continued and is currently filled by the Military Aides to the President. These roles carry a wide variety of responsibilities, from critical military command and control missions to ceremonial duties at Presidential events. The White House Garage was created by an act of Congress in 1909. Over the years it was transformed into a military organization and became a regular unit in 1963 by the name of the U.S. Army Transportation Agency (White House). It was later renamed the White House Transportation Agency.

Camp David was established in 1942 to provide the President a safe and relaxing residence away from the White House. That same year, the White House Communications Agency was formed to assure that the President always had access to safe, secure, and reliable means of communication. Two years later, President Franklin D. Roosevelt called for the creation of the Presidential Pilot's Office (renamed the Presidential Airlift Group in 2001) to provide air transportation to the President and his staff.

The White House Medical Unit was established in the West Wing in 1945. The White House Mess was established in 1951 and has been run by the Navy ever since. Marine Helicopter Squadron One (HMX-1) was created in 1957 when President Dwight D. Eisenhower was vacationing in Newport, Rhode Island, and had to return to the White House on short notice. He flew the first portion of the trip aboard HMX-1.