Marine Fighter Attack Squadron 251 was activated in December 1941 at NAS North Island, California. Known as the Marine Observation Squadron 251, the Thunderbolts flew the Grumman F-4F "Wildcat" in numerous Pacific campaigns during World War II.
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With the outbreak of the Korean War in 1950, VMF-251 was directed to transition to the AD-4D "Skyraider." The squadron moved to Korea in June 1953 and had the distinction of flying the last Marine combat mission of the war.
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In 1960, VMF-251 was assigned to Marine Aircraft Group 31 at MCAS Beaufort, South Carolina. During this period, VMF-251 was the first Marine F-8 squadron to deploy aboard an aircraft carrier as part of Carrier Air Wing 8.
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During January 1986, the Thunderbolts transitioned to the F/A-18 Hornet. The following August the squadron stood up as the sixth Marine F/A-18 squadron and reported fully to combat in March 1987. Over the next 6 years, the squadron participated in the WESTPAC rotation program, completing 3 six-month deployments to Iwakuni, Japan flying the F/A-18 Hornet. From January 1994 to April 1994, the Thunderbolts participated in close air support combat missions while deployed to Aviano, Italy in support of the United Nations peacekeeping efforts in Bosnia-Herzegovina. These missions marked the only combat sorties for a Marine squadron in Europe since World War I.
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From August 1995 to February 1996, the squadron flew combat and contingency sorties during Operations Deny Flight, Joint Endeavor, Decisive Edge and Southern Watch. For its performance, VMFA-251 was nominated for the Commandants Aviation Trophy.