Constituted as the 487th Fighter Squadron on 29 September 1942, it was assigned to the 352nd Fighter Group.  The squadron's first home was at Mitchel Field, New York, followed by durations of about a month at each of the following bases: Bradley Field, Connecticut; Westover Field, Massachusetts, Trumbull Field, Connecticut; back to Mitchel Field, New York; and finally Bodney in England on 7 July 1943. In December 1944 the Group moved from Bodney to airfields Y29 at Asch, and then to A84 at Chievres, Belgium.

The squadron flew P-47 Thunderbolts until early 1944, switching to the P-51 Mustang until the end of the war. It took part in several campaigns: Air Offensive, Europe; Normandy; Northern France; Rhineland; Ardennes-Alsace; and Central Europe.

Squadron decorations including the Distinguished Unit Citation and the French Croix de Guerre with Palm. The Group also produced the highest scoring 'Mustang Ace' of the war, Major George E. Preddy, Jr. The three squadrons of the 352nd Fighter Group were nicknamed 'The Blue Nosed Bastards of Bodney', referring to the distinctive blue paint job adorning the Mustangs' nose and upper cowling.

The 487th Fighter Squadron was known as 'Meyer's Maulers' after its high-ranking ace and commanding officer John C. Meyer.

The character depicted on the emblem was called 'Lil Bastard'. The squadron artist Sgt. Sam Perry did a brilliant job in bringing to life this most determined-looking and pugnacious little fighter. The squadron was inactivated on 10 November 1945.