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The Type 35 was phenomenally successful, winning over 1,000 races in its time. It took the Grand Prix World Championship in 1926 after winning 351 races and setting 47 records in the two prior years. At its height the Type 35 averaged 14 race wins per week. Bugatti won the Targa Florio for five consecutive years, from 1925 through 1929, with the Type 35.

The Bugatti Type 35 was continually being modified and improved upon, but retained the same chassis and body style with primarily just engine changes unless otherwise noted. They broadly fall into the following nomenclature:

Type 35 

This original, defining model was introduced at the 1924 French Grand Prix, held at Lyon. 

The car used an evolution of the three-valve 2.0 L overhead cam straight-eight engine first seen on the Type 29. 

This new powerplant featured a sophisticated roller bearing system, numbering five in total. This allowed the engine to rev to 6,000 rpm. Output was up to 90 hp. Alloy wheels were a novelty, as was the hollow front axle for reduced unsprung weight. 

96 of these un-supercharged T35 examples were produced.

Type 35A

A mechanically simpler version of the Type 35 appeared in May 1925. Intended for road use while retaining the 'racing look', several were raced anyway and with some success. The engine used plain bearings on the crankshaft (for ease of maintenance), smaller valves, and coil ignition, it was normally delivered on regular wire-spoked wheels.

139 examples of the Type 35A were produced.

Type 35T

Bugatti introduced a special model for the 1926 Targa Florio race with engine displacement set to 2.3 L, the car could not be used at a Grand Prix due to rules limiting capacity to 2.0 L.

13 T35Ts were produced.

Type 35C

The Type 35C was introduced in 1926 and featured a Roots supercharger, despite Ettore Bugatti's disdain for forced induction. Output was nearly 128 hp with a single Zenith carburettor. The Type 35C came first and second during its first race outing at the 1926 Milan Grand Prix held at Monza. This 2 litre supercharged configuration continued to be very dependable.

45 T35Cs were produced.

Type 35B 

Named by the factory "Type 35TC" (Targa Compressor), this most powerful version became known colloquially as the "T35B". It shared the 2.3 L engine of the Type 35T this time with a large supercharger added. Output was 138 hp. A British Racing Green Type 35B driven by William Grover-Williams won the inaugural 1929 Monaco Grand Prix.

37 Type 35B were produced.

Type 37

The Type 37 sports car used the same chassis and bodywork as the full-power Type 35, but were mostly delivered with wire wheels. Fitted with a new 1.5 L 4-cylinder engine, it was easier to maintain for many privateer drivers. This engine was a SOHC three-valve design and produced 60 hp. 

223 Type 37s were built.

Type 37A

The supercharged Type 37A enabled engine output to reach 80–90 bhp. It also had larger shrouded brake drums.

67 Type 37As were produced.

Type 39

The Type 39 was similar to the Type 35 except for the engine crankshaft, modified to produce a smaller 1.5 L. Stroke was down from 88 mm to 66 mm, and a mix of plain and roller bearings were used in the crank.

10 examples were produced (some being supercharged (Type 39A)).

Type 51

The Bugatti Type 51 series succeeded the famous Type 35 as Bugatti's premier racing car for the 1930s. The main distinction is that it uses a twin cam engine. Unlike the dominant Type 35s of the prior decade, the Type 51 (and later Type 53, Type 54, and Type 59) were unable to compete with the government-supported German and Italian offerings.​

The first Type 51 went into production in 1931 with Ettore Bugatti's son Jean Bugatti taking more responsibility. Its engine was a 160 hp twin overhead cam evolution of the supercharged 2.3 L single overhead cam straight-8 found in the Type 35B. 

A victory in the 1931 French Grand Prix was a good start for the type, and it notably won the 1933 Monaco Grand Prix with Achille Varzi beating Tazio Nuvolari in a Homeric struggle against the new challenge of the Alfa Romeo 8C.

The Type 51 is visually very similar to the Type 35. 

40 examples of the Type 51 and 51A were produced.

Type 54

As a stop gap between planned models, Bugatti produced the Type 54. It became a synthesis of the Type 45 chassis with an eight-cylinder engine from the Type 50. It was raced actively from 1930 to 1933 and became known for its brute power among the more nimble Type 35s it replaced. At the Monza GP in 1930, Louis Chiron and Archille Varzi raced the first two Type 54s. Varzi was able to secure third place which wasn’t bad for a car conceived and fabricated in just two weeks. A highlight victory came when Varzi won at at Avus in 1933.