Initially under USAAC, the name of the facility was Municipal Airport, Dover Airdrome and the airfield opened on 17 December 1941.

On 20 December the first military unit arrived at Dover's new airfield: the 112th Observation Squadron of the Ohio National Guard which flew anti-submarine patrols off the Delaware Coast.

The antisubmarine mission ended on 6 June, and construction crews moved back to the base for a major upgrading project that lengthened the main runway to 7,000 feet.

During the construction period and continuing into June 1944, Dover AAB became a sub-base of Camp Springs Army Airfield, Maryland.

Full operational capability was restored to Dover in September, and seven P-47 Thunderbolt squadrons arrived for training in preparation for eventual involvement in the European Theater, while the 83d Fighter Group was assigned to Dover as the Operational Training Unit, The 83rd was redesignated the 125th Base Unit on 10 April 1944, with very little change in its mission.

In 1944, the Air Technical Service Command chose Dover as a site to engineer, develop, and conduct classified air-launched rocket tests.

The information collected during these experiments resulted in the effective deployment of air-to-surface rockets in both the European and Pacific combat theaters.

On 1 September 1946, as a result of the drawdown of United States forces after the war, Dover Army Airfield was placed on temporary inactive status.

A small housekeeping unit, the 4404th Base Standby Squadron, remained on the airfield for care and maintenance of the facility.

During the 1950s problems developed with many of the facilities in Dover, which had been hastily constructed to support its World War II mission.

That year, Dover AFB was also used to store hundreds of bodies from the mass murder and suicide of the Jonestown community in Guyana.

[4][5] Some of the more memorable flights during the post-war period included the airdrop and test firing of a Minuteman I intercontinental ballistic missile and the delivery of a 40-ton superconducting magnet to Moscow during the Cold War, for which the crew received the Mackay Trophy.

[6] In March 1989, C-5s from Dover delivered special equipment used to clean up the Exxon Valdez oil spill in Prince William Sound, Alaska.

On June 7, 1989, while attending the Airlift Rodeo, a 436 MAW C-5 set a world record when it airdropped 190,346 pounds and 73 paratroopers.

During Desert Shield, the wing flew approximately 17,000 flying hours and airlifted a total of 131,275 tons of cargo in support of combat operations after the Iraqi invasion of Kuwait.

Their remains are processed, inspected for unexploded ordnance, cleaned, and prepared for burial before being escorted to the point of interment decided by the family.

In 2009 the base received a new 128-foot tall tower, overlapping the original 103-foot one which was donated to the Air Mobility Command Museum, accessible to visitors.

The Charles C. Carson Center for Mortuary Affairs has also been used to identify remains of civilians in certain exceptional circumstances: in 1978 for the victims of the Jonestown mass murder/suicide, in 1986 for identifying the remains of the crew of the Space Shuttle Challenger, and in 2003 for the crew of the Space Shuttle Columbia.

Two sections of the 436th Aerial Port Squadron warehouse collapsed on February 18, 2003, as a result of a record snow storm.

According to the United States Census Bureau, Dover Base Housing has a total area of 0.7 square miles (1.7 km2), all land.

Eagle Heights Family Housing contains a total of 19,500 feet (5,900 m) of greenbelt paths for walking, jogging, and biking.

Tours are conducted during the day by volunteers, many of whom are retired pilots, navigators, flight engineers and loadmasters who provide first-person narratives of actual events.

The museum also maintains archives related to the history of the Air Mobility Command and Dover AFB.

Building 1301, Dover Air Force Base was added to the National Register of Historic Places in 1994.

A single battered Douglas C-47A Skytrain, salvaged in 1986 off of a dump at Olmsted Air Force Base, near Harrisburg, Pennsylvania, after being used for target practice, was the museum's modest beginning.

Airlifted to Dover AFB by a Pennsylvania National Guard helicopter, "It was the first aircraft restored for the newly conceptualized museum that would form here."

Founded as the Dover AFB Historical Center on 13 October 1986, it originally was housed in three hangars within the main area of the base.