The 400th was activated in spring 1942 as a B-26 Marauder medium bomber squadron, training under the Third Air Force in the southeastern United States. They were reassigned to Michigan, receiving Very Long Range (VLR) B-24D Liberator heavy bombers manufactured by Ford for extended length missions over the Pacific.
The squadron was deployed first to Hawaii and trained on the heavy bombers for combat and long over ocean navigation and bombardment missions under Seventh Air Force, then deployed to the Fifth Air Force in the Southwest Pacific Area (SWPA), assembling in northern Queensland, Australia then moving to an operational base in Papua New Guinea. From airfields in New Guinea, the squadron carried out long-range strategic bombardment of enemy targets in New Guinea, Dutch East Indies, Philippine Islands and other areas from bases as ground forces sized them during MacArthur’s island hopping campaign.
The squadron bombarded enemy targets on Okinawa; Iwo Jima; Formosa and eastern China, eventually being stationed on Ie Shima preparing for VLR bombardment operations over the Japanese Home Islands when the Japanese Capitulation occurred in August 1945. Squadron personnel were demobilized in Okinawa and Philippines, and the aircraft sent to reclamation during the fall of 1945. Inactivation followed in early 1946.
The squadron was reactivated on 1 July 1964 as an ICBM squadron assigned to the 90th Missile Wing at Francis E. Warren AFB, Wyoming, and equipped with 50 LGM-30B Minuteman Is in early 1964, then upgraded to LGM-30G Minuteman III in 1973/1974. It received 50 LGM-118A Peacekeeper ICBMs in 1986, the only USAF missile squadron to put them on operational alert. Inactivation of Peacekeepers began in 2001, and the last missile was inactivated in 2005. Squadron inactivation followed on 19 September 2005.