Capt. (later Sir) Geoffrey de Haviland designed the D.H. 4 in response to a specific request for a day-bomber. It was the first British aircraft to be designed for this specific application. The construction was of typical fashion for the time, being of wood with cross-wire bracing and fabric covering. One unique aspect of the design was that the fuselage was of a box-girder configuration with cross-bracing only in the four bays immediately behind the rear cockpit. Forwards of that point the fuselage was covered in 3mm plywood. The wings had two spruce spars and had ailerons on the upper wings.

The prototype first flew in mid-August 1916. Formal testing occurred between 21 September to 12 October 1916. An example of the machine went to France on 15 October for service trials. Originally intended to be powered by a 230 hp BHP Galloway, Adriatic engine the machine went through a wide variety of power plants before the 375 hp Rolls-Royce Eagle engine was selected as the power plant of choice. Armament and ordinance for the aircraft consisted of one 0.303 in. Vickers machine gun for the pilot (early RNAS machines had twin Vickers) and one 0.303 in. Lewis machine gun, on either a double yoked pair or a Scarff ring mounting for the Observer). Two 230-lb. bombs or four 112-lb. bombs were carried. Formal introduction into a service squadron occurred on 6 March 1917 when No. 55 Squadron went to France.

At the time of entry into the war the American Air Service lacked aircraft suitable for service on the Western Front. They therefore procured various aircraft from the British and French. One such aircraft obtained with the British D.H. 4. Squadrons assigned this machine were: the 8th Observation Squadron; the 11th Aero Squadron; the 20th Aero Squadron; the 50th Observation Squadron; the 85th Observation Squadron; the 96th Aero Squadron (a few machines); the 100th Aero Squadron; the 135th Aero Squadron; the 155th Observation Squadron; the 166th Aero Squadron; the 168th Observation Squadron; the 278th Observation Squadron; and the 354th Observation Squadron. In addition, the First Marine Aviation Force flew the D.H. 4 as part of its role as the day-wing of the Navy's Northern Bombing Group.

1st. Lt. Harold E. Goettler and 2nd Lt. Erwin R. Bleckley of the 50th Aero Squadron, flying a D.H. 4, were awarded the Congressional Medal of Honor for their efforts in attempting to drop supplies to the Lost Battalion in September 1918.