Upon the entry of the United States into the war there was a great deal of uncertainty just what the aviation needs of the military were to be. A study-group, called the Bolling Commission proceeded to Europe to evaluate the aviation situation and to make recommendations related to the procurement and production of aircraft. In a cable of 28 June 1917 the Commission recommended that the U.S. procure the British D.H. 9 aircraft for long-range bombing activities and the British D.H. 4 for training purposes. The D.H. 4 was selected for production in July 1917.

The first example of a D.H. 4 arrived in the United States from England, without a powerplant, on 27 July 1917 and the first aircraft was produced on 29 October 1917. On 5 September the Aircraft Production Board ordered 2000 D.H. 9 machines to be powered by the new Liberty V-12 engine, rated at 400 hp. On 25 January 1918 this order was changed from the D.H. 9 design to the D.H. 4 design due to unsettled conditions relating to the D.H. 9 design to permit production.

The first American built D.H. 4 was delivered to the U.S. Air Service in February 1918. It appeared in France 11 May 1918. However, due to problems with its construction the first flight over the lines did not happen until 9 August 1918 (most likely date as other dates of 2, 7, and 8 August are also quoted). By the end of the war some 3431 machines had been built, 1213 had been delivered to France, and 196 machines had been assigned to 12 Air Service squadrons as well as to the First Marine Aviation Force of the Navy's Northern Bombing Group.

The first squadron to receive the machine was the 135^th Aero Squadron. It was initially assigned the role of a fighter aircraft (because of its speed relative to the German fighters it was facing) for Spad's assigned to ground attack work. The fallacy of this role was soon recognized and it returned to its intended role as an observation/day-bomber machine. The principle difference between the American and British versions of the D.H. 4 lay in the power plant used in the American version. Because of the increased weight of the Liberty V-12 some strengthening of the fuselage was required. Also, the pilot's Vicker's gun was replaced by a pair of Marlin machine, which in turn was latter replaced by Browning machine guns. The Observer retained his pair of Vickers guns. The maximum bomb load of the American machine was 12 bombs of a weight not to exceed 322 lbs. in any combination.

2^nd Lt. Ralph Talbot and Gunnery Sgt. Robert Guy Robinson of the 1^st Marine Aviation Force of the Northern Bombing Group were awarded the Congressional Medal of Honor for action, in an American D.H. 4, on October 14, 1918.