Construction began at Honington in 1935. The contractor was John Laing and Son, the same firm that would later build sections of the M1 motorway and Coventry Cathedral. The station opened on 3 May 1937, just as Britain began rearming in earnest. Bomber Command moved squadrons through quickly: 77 Squadron with Hawker Harts, 102 Squadron with Handley Page Heyfords, 75 Squadron with the new Vickers Wellington. By September 1939, IX Squadron and its Wellingtons were waiting on the apron when the Prime Minister told the country, in a flat exhausted voice on the BBC, that no such undertaking had been received and consequently this country was at war with Germany. They flew the next day.

In May 1941, a Wellington returning from a night sortie tried to land at Honington with its wheels still retracted. It skidded sideways into the main bomb dump and burst into flames. The trapped aircrew were going to burn alive. Group Captain J. A. Gray, the station commander, and Squadron Leader Aidan MacCarthy, the station medical officer, arrived first at the wreck. Both men climbed into the burning aircraft. Between them they pulled two of the crew clear before the heat drove them back. The bombs cooked off shortly after. Gray and MacCarthy were each awarded the George Medal for civilian gallantry. MacCarthy would later survive Japanese prison camps after the fall of Java, and his memoir A Doctor's War became a quiet classic. He kept his George Medal for the rest of his life.

In June 1942 the United States Army Air Forces took over the station and upgraded it to Class A bomber base specification, calling it Station 375. Eventually the 364th Fighter Group flew P-38 Lightnings, then P-51 Mustangs from Honington. They escorted B-17s deep into Germany, strafed targets across France and the Low Countries, supported the Normandy invasion in June 1944, took part in Operation Market Garden in September, and helped hold the line during the Battle of the Bulge that winter. The aerial photograph of Honington taken on 25 January 1944 shows dozens of Fortresses parked on hardstands across the field, ground crews scrambling over them. The First Strategic Air Depot was based here too, repairing battle-damaged B-17s and sending them back into the fight.

After the war, Honington went through several reinventions. RAF Transport Command used it to support the Berlin Airlift in 1948-49. A 9,000-foot concrete runway was laid down in 1956, long enough for jet bombers. From 1969 the station became home to Hawker Siddeley Buccaneers, low-level maritime strike aircraft originally built for the Royal Navy. Squadrons 12, 15, 16, 208 and 216 flew Buccaneers from Honington at one time or another. The runway pointed east, toward the Warsaw Pact. When the Cold War ended and the Buccaneers retired, Honington's flying days ended too. The last flying squadron departed on 1 February 1994. Honington's station badge, awarded in 1956, carries the head of St Edmund and two crossed arrows pointing downward, taken from the coat of arms of Bury St Edmunds nine kilometres to the southeast. The arrows in saltire represent Edmund's martyrdom by the Vikings.

In June 1994, the RAF Regiment depot moved here from RAF Catterick in Yorkshire. Honington became, and remains, the central hub for protecting RAF bases worldwide. Over 1,500 personnel work here. Three field squadrons of the RAF Regiment train and deploy from the station. The RAF Police headquarters is here. The RAF Force Protection Centre teaches everything from convoy security to airfield defence against chemical, biological and radiological threats. The station motto is Pro anglia valens, Valiant for England. Honington is also home to the British Army's 28 Engineer Regiment, who took over the CBRN defence role in 2019, and a flying club with a single Piper PA-28. After 88 years, the airfield where the war began still does what it was built for: it protects the country.