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The origin of the Do 335 goes back to World War I when Claude Dornier designed a number of flying boats with tandem engines. These were used on most of the multi-engined Dornier flying boats that followed, including the highly successful Do J Wal and the gigantic Do X. The main advantage of this arrangement is the reduced drag due to the smaller frontal area. It also keeps the weight of the twin powerplants near, or on, the aircraft centerline, increasing the roll rate compared to a traditional twin. In addition, a single engine failure does not lead to asymmetric thrust, and in normal flight there is no net torque, so the aircraft is easier to handle. The ventral fin–rudder of the cruciform tail protected the rear propeller from accidentally striking on takeoff. The presence of the rear pusher propeller also necessitated the provision for an ejection seat for safe escape from a damaged aircraft, and designing the rear propeller and dorsal fin mounts to use explosive bolts to jettison them before an ejection was attempted – as well as twin canopy jettison levers, one per side[3] located to either side of the forward cockpit interior just below the sills of the five-panel windscreen's sides, to jettison the canopy from atop the cockpit before ejection.[4]

In 1939, Dornier, reviving a principle he had patented in 1937,[5] was working on the P.59 high-speed bomber project, which used the tandem engine layout. In 1940, he commissioned a test aircraft, closely modeled on the airframe of the early versions of the Dornier Do 17 bomber but only 40% of the size, with no aerodynamic bodies of any sort on the wing panels (the Do 17 had twin engine nacelles on its wings) and fitted with a retractable tricycle landing gear to validate his concept for turning the rear pusher propeller with an engine located far away from it, through the use of a long tubular driveshaft. This aircraft, the Göppingen Gö 9,[6] showed no unforeseen difficulties with this arrangement, but work on the P.59 was stopped in early 1940 when Hermann Göring[citation needed] ordered the cancellation of all projects that would not be completed within a year or so.

In May 1942, Dornier submitted an updated version with a 1,000 kg (2,200 lb) bomb load as the P.231, in response to a requirement for a single seat, Schnellbomber-like high-speed bomber/intruder. The P.231 proposal was selected as the winner after beating rival designs from Arado, Junkers, and Blohm & Voss. A development contract was awarded, by the RLM issuing the Dornier firm the airframe approval number 8-335, for what would become known as the Do 335. In autumn 1942, Dornier was told that the Do 335 was no longer required, and instead a multi-role fighter based on the same general layout would be accepted. This delayed the prototype delivery as it was modified for the new roll

When fitted with DB 603A engines delivering 1,750 PS (1,290 kW; 1,730 hp) it had a pair of the largest inverted V12 aircraft engines mass-produced during the Third Reich's existence. The Do 335 V1 first prototype CP+UA, flew on 26 October 1943 under the control of Flugkapitän Hans Dieterle, a regular Heinkel test pilot and later primary Dornier test pilot. However, several problems during the initial flight of the Do 335 would continue to plague the aircraft through most of its short history. Issues were found with the weak landing gear and with the main gear's wheel well doors, resulting in them being removed for the remainder of the V1's test flights. The Do 335 V1 made 27 flights, flown by three different pilots. During these test flights the second prototype, V2 (Werk Nr 230002) CP+UB, was completed and made its first flight on 31 December 1943, again under the control of Dieterle. New to the V2 were upgraded DB 603A-2 engines, and several refinements learned from the test flights of the V1 as well as further windtunnel testing. On 20 January 1944, the Do 335 V3 (W.Nr. 230004), CP+UC was completed and flown for its first time by Werner Altrogge. The V3 was powered by the new pre-production DB 603G-0 engines which could produce 1,900 PS (1,400 kW) at take-off and featured a slightly redesigned canopy which included twin rear-view mirrors in blisters, one in each of two matching side panels of the well-framed, eleven-panel main canopy's openable section. Following the flights of the V3, in mid January 1944, RLM ordered five more prototypes (V21–V25), to be built as night fighters. By this time, more than 60 hours of flight time had been put on the Do 335 and reports showed it to be a good handling, but more importantly, very fast aircraft, described by Generalfeldmarschall Erhard Milch himself as "...holding its own in speed and altitude with the P-38 and it does not suffer from engine reliability issues". The Do 335 was scheduled to begin mass construction, with the initial order of 120 preproduction aircraft to be manufactured by Dornier-Werke Friedrichshafen (DWF) to be completed no later than March 1946. This number included a number of bombers, destroyers (heavy fighters), and several yet to be developed variants. At the same time, Dornier-Werke München (DWM) was scheduled to build over 2,000 Do 335s in various models, due for delivery in March 1946 as well.

On 23 May 1944, Hitler, as part of the developing Jägernotprogramm (Emergency Fighter Program) directive, which took effect on 3 July, ordered maximum priority to be given to Do 335 production. The main production line was intended to be at Manzell, but a bombing raid in March destroyed the tooling and forced Dornier to set up a new line at Oberpfaffenhofen. The decision was made, along with the rapid shut-down of many other military aircraft development programs, to cancel the Heinkel He 219 night fighter, which also used the DB 603 engines (in well-unitized installations), and use its production facilities for the Do 335 as well. However, Ernst Heinkel managed to delay, and eventually ignore, its implementation, continuing to produce examples of the He 219A.

At least 16 prototype Do 335s were known to have flown (V1–V12, W.Nr 230001-230012 and Muster-series prototypes M13–M17, W.Nr 230013–230017) on a number of DB603 engine subtypes including the DB 603A, A-2, G-0, E and E-1. The first preproduction Do 335 (A-0s) starting with W.Nr 240101, Stammkennzeichen VG+PG, were delivered in July 1944. Approximately 22 preproduction aircraft were thought to have been completed and flown before the end of the war, including approximately 11 A-0s converted to A-11s for training purposes. One such aircraft was transferred to the Royal Aircraft Establishment at Farnborough, and later, after a rear-engine fire burnt through the elevator controls during a flight, crashed onto a local school.[7]

The first 10 Do 335 A-0s were delivered for testing in May 1944. Do 335 V3, (T9+ZH), W.Nr. 230003 was delivered to the Luftwaffe's experimental reconnaissance unit, 1./Versuchsverband OKL, in late May. However, it suffered constant problems and was returned to Dornier in September.[8] By late 1944, the Do 335 A-1 was on the production line. It was similar to the A-0 but with the uprated DB 603E-1 engines of around 1,324 kW (1,776 hp) take-off power rating on 87 octane fuel,[9] and two underwing hardpoints for additional bombs, drop tanks or guns. It had a maximum speed of 763 km/h  at 6,500 m  with MW 50 boost, or 686 km/h  without boost, and climbed to 8,000 m in under 15 minutes. Even with one engine out, it reached about 563 km/
Delivery commenced in January 1945. When the United States Army overran the Oberpfaffenhofen factory in late April 1945, only 11 Do 335 A-1 single-seat fighter-bombers and two Do 335 A-12 trainers had been completed. The two-seater trainer version was called Ameisenbär ("anteater").

French ace Pierre Clostermann claimed the first Allied combat encounter with a Pfeil in April 1945. He described leading a flight of four Hawker Tempests from No. 3 Squadron RAF over northern Germany when they came across an unknown aircraft whose description matched the Do 335's, flying at maximum speed at treetop level. Detecting the British aircraft, the German pilot reversed course to evade. Two pilots fired on the Dornier but Clostermann, despite the Tempests' considerable low altitude speed, decided not to attempt to chase it as it was obviously much faster.

On 26 April 1945, the Do 335 V9, which was still at Rechlin, was test-flown by Oberleutnant Heinrich Schild. Later that day he escorted Hanna Reitsch and General der Flieger Robert von Greim's flight to Berlin-Gatow. After arriving at Gatow, Reitsch and von Greim commandeered a Fieseler Fi 156 Storch and flew to Hitler's bunker. Also on 26 April, Fliegerstabsing. Heinz Fischer attempted to fly Do 335 V9 from Rechlin to Switzerland. Due to a compass failure, he strayed over France and ran out of fuel. Both the ejector seat and the tail jettison mechanism failed and he had to bail out over the Vosges mountains.