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The genesis of the DB-3 lay in the BB-2, Sergey Ilyushin's failed competitor to the Tupolev SB. Ilyushin was able to salvage the work and time invested in the BB-2's design by recasting it as a long-range bomber, again competing against a Tupolev design, the DB-2, to meet the stringent requirements of an aircraft capable of delivering a 1,000 kg  bombload to a range of 3,000 km  at a maximum speed no less than 350 km/h . He had redesigned the BB-2 to take advantage of the radial Gnome-Rhône Mistral Major 14Kdrs engine, for which the Soviets had purchased a license in 1934 as the M-85, and had begun construction of the prototype of the BB-2 2K-14 as the TsKB-26 that same year.

The TsKB-26 was more of a proof-of-concept vehicle to validate Ilyushin's ideas on how to obtain long range than an actual bomber prototype. To speed the construction process, it had a wooden fuselage and fin with metal wings and tail surfaces. It made its first flight in the summer of 1935 and proved to be stable, easily controllable and highly maneuverable; it performed the first loop made by a twin-engined aircraft in the Soviet Union. It went on to set six world records in its class, generally in payloads to height and speed over a 5,000 km  closed circuit.

The real prototype of the DB-3 was called the TsKB-30 and it was completed in March 1936. It had a number of improvements over the TsKB-26, notably an all-metal structure, an extended nose, an aft-sliding canopy with a fixed windscreen and improved engine cowlings. It passed the State acceptance trials and was ordered into production in August 1936 as the DB-3, although some sources refer to this initial series as the DB-3S for seriynyy (series-built).

The DB-3 was not a simple or easy aircraft to manufacture as Ilyushin had pushed the limits of the available construction technology to make it as light as possible. For example, the spar in each wing panel had four parts which had to be riveted together and there were numerous welds that each had to be inspected by an X-ray machine, with many failures. In addition the internal riveting of small-diameter tubing was also a difficult and time-consuming process

The bomb bay was designed to carry ten 100 kg  FAB-100 bombs, but heavier bombs could be accommodated on external bomb racks up to a total of 2,500 kg  on short-range missions. The defensive armament for the three crewmen consisted of three 7.62 mm  ShKAS machine guns. One in the tip of the nose manned by the bombardier-navigator and the two others protecting the rear. The rear gunner manned both the gun in the SU dorsal turret and the gun in an LU ventral hatch

Flight tests of the second example pre-production aircraft, conducted May–October 1937, revealed that it was slightly inferior to the TsKB-30 in performance, but still exceeded its requirements by a considerable margin. It attained a speed of 390 km/h  at an altitude of 5,000 m . It could carry a bombload of 500 kg  to a range of 4,000 km  and a 1,000 kg  bombload to a range of 3,100 km . In comparison, the Heinkel He 111B then in production was 10–20 km/h  slower and could carry only 750 kg  of bombs to a range of 1,660 km  and 1,500 kg  to a distance of 910 km . This performance arguably made it the best twin-engined bomber in the world already or entering service in 1937. 45 DB-3s were built that year at Factory No. 39 in Moscow and No. 18 in Voronezh and the aircraft entered service with the VVS.

During 1938 the improved M-86 engine, rated at 950 horsepower (710 kW) for takeoff, replaced the M-85 on the production line. Aircraft with this engine are properly referred to as DB-3 2M-86, but are sometimes referred to as the DB-3A, after the three-step upgrade program planned for the aircraft. Other minor changes were introduced over the course of the year. Factory No. 126 in Komsomolsk-on-Amur also began producing DB-3s in 1938

During 1938–39 the Tumansky M-87A engine was introduced on the production line in a gradual transition as were VISh-3 variable-pitch propellers. The M-87 had the same horsepower rating at takeoff as the M-86, but produced more power at higher altitudes. The M-87B further increased power at altitude and was introduced in 1939–40. These aircraft were known as the DB-3B as part of the second stage of the upgrade program. The last production batches in 1940 had the Tumansky M-88 that produced 1,100 horsepower (820 kW) for takeoff. These increased the maximum speed to 429 km/h  at 6,800 metres
In 1939, 30 DB-3s were supplied to the Republic of China Air Force during the Second Sino-Japanese War and they saw heavy action against Japanese targets in the Wuhan region from their bases in Sichuan (mostly used by the 8th Group), before being replaced by B-24 Liberators in 1943.

Two DB-3s were responsible for shooting down the neutral Finnish civilian Junkers Ju 52 passenger and transport plane Kaleva on June 14, 1940.

The Finns captured five force-landed DB-3Ms during the Winter War and during 1941 they purchased a further six DB-3Ms and four DB-3F/Il-4s from German surplus stocks.

On the night of August 7-8, 1941, fifteen DB-3T torpedo bombers of the Baltic Fleet dropped the first Soviet bombs on Berlin. From August 11, DB-3Fs of the VVS resumed bombing.

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