Air Force mortuary missions have been attached to many organizations and locations over the years. The mortuary mission in Delaware dates back to 1955, when the Port Mortuary was established at Dover Air Force Base, Delaware. Prior to the establishment of AFMAO, the port mortuary at Dover was a flight under the 436th Services Squadron. In 2001, the Dover Port Mortuary became the sole port mortuary in the continental U.S. after the mortuary at Travis Air Force Base in California closed. AFMAO became a named activity of the Headquarters Air Force, Deputy Chief of Staff, Personnel, Services and Manpower Dec. 15, 2008. Shortly thereafter, the Headquarters Air Force Mortuary Affairs function transferred from the Air Force Services Agency, San Antonio, Texas to join the new organization. AFMAO became a Field Operating Agency May 1, 2014, aligning it directly under Headquarters Air Force leadership.
In 2010, Operating Location Europe was established at Ramstein Air Base, Germany. In June 2019, Operating Location Pacific was established at Hickam Field, Joint Base Pearl Harbor-Hickam on Oahu, Hawaii. In January 2020, AFMAO assumed administrative and operational control of OLP-Yokota, located at Yokota Air Base, Japan.