The museum's origin story has the scrappy charm of an underdog. It opened on 22 June 1974 inside a converted 1940s-era chapel on Eglin Air Force Base. Two years later, the Air Force Armament Museum Foundation was established to raise money for a proper building. But the effort ran into fierce local opposition: a county referendum to fund the new structure failed outright. The original chapel building was condemned in 1981, forcing the museum to close its doors entirely. For four years, the collection sat in limbo. When the new building finally opened on 15 November 1985, the museum wasted no time filling it. A prisoner-of-war exhibit was inaugurated shortly after. Then the aircraft started arriving in rapid succession: an SR-71 Blackbird in 1990, a B-52 Stratofortress in 1991, and a Soviet-built MiG-21 in 1992. An exhibit honoring Air Force Special Operations Command followed in 1996.

The museum's exhibits read like a catalog of escalating destructive capability. The ordnance collection includes the AMRAAM air-to-air missile, the GBU-28 bunker-buster developed during Operation Desert Storm, Paveway laser-guided bombs, Tomahawk cruise missiles, and the Hound Dog standoff missile. The T-12 Cloudmaker earthquake bomb stands outside, a relic of an era when sheer explosive mass was the answer to hardened targets. Inside, a gun vault displays weapons spanning centuries of infantry combat, from a 1903 Springfield rifle to the GAU-8 Avenger cannon -- the same seven-barrel rotary gun built around the A-10 Warthog, capable of spitting 6,000 rounds per minute. The Sikes Antique Pistol Collection adds an unexpected grace note: over 180 handguns including flintlocks, dueling pistols, Western six-shooters, and Civil War-era sidearms.

The outdoor aircraft display forms a timeline of American military aviation. A World War II-era B-17G Flying Fortress and P-47N Thunderbolt stand alongside Cold War workhorses like the F-104 Starfighter and F-105 Thunderchief. The SR-71A Blackbird, serial number 61-7959, remains one of the collection's crown jewels -- a reconnaissance aircraft that once flew at speeds exceeding Mach 3. A B-52G Stratofortress nicknamed "El Lobo II" was repainted in April 2022 after decades of Florida sun and salt air. In 2019 and 2020, the museum experimented with wrapping a P-51 Mustang and an F-86 Sabre in vinyl to protect them from the elements, a modern preservation technique applied to mid-century machines. The collection also includes a Sikorsky MH-53M Pave Low IV special operations helicopter and an AC-130A Spectre gunship, aircraft that represent the quieter, more dangerous end of air warfare.

The museum continues to expand. Following decades of planning, an African American Military Heritage Hall opened in February 2022 as the first of four planned Quonset hut-styled structures. A BLU-82B "Daisy Cutter" bomb was acquired in 2019, adding yet another piece of ordnance history. In May 2024, a new visitor control center for Eglin Air Force Base opened on the museum grounds, reflecting the facility's dual role as both a public attraction and a gateway to one of the largest military installations in the western world. The museum also hosts the Engineers for America education program, bringing local school children through for hands-on engineering experiments among the bombs and fighters. Admission remains free, supported by the nonprofit Air Force Armament Museum Foundation that fought so hard for the museum's existence half a century ago.