During World War II he served in the Royal Australian Air Force. In 1946 he opened a small repair business. He also raced midget cars and in his first season won the New South Wales Championship and formed a partnership with Ron Tauranac.
In 1955 he made his Grand Prix debut at the British Grand Prix driving his own Maserati 250F. He soon joined the Cooper Car Company team, which was the first to run the engine at the rear. In 1959 Brabham won the World Championship with a Coventry Climax engined Cooper. In 1960 he won the championship again with Cooper.
Brabham took the Championship-winning Cooper to the Indianapolis Motor Speedway for a test following the 1960 season, then entered the famous Indianapolis 500 in a modified version of the Formula One car in 1961. The "funny" little car from Europe was mocked by the other teams, but it ran as high as third and finished ninth. The Indianapolis establishment gradually realized the writing was on the wall as Brabham and his team principal John Cooper had shown that the days of front-engined roadsters were numbered. Ironically, Cooper were not as competitive this year, as the 1.5 litre engine rules were introduced and the famous Shark Nose Ferrari dominated. Brabham also raced at Indy in 1964, 1969 and 1970.
In 1961 he founded the Brabham Racing Organisation with Ron Tauranac. A newly introduced engine limit in Formula One of 1500cc did not suit Brabham and he did not win a single race with a 1500cc car, although his first team win came in 1964 with driver Dan Gurney. In 1966 a new 3000cc formula was created, Brabham in a Brabham-Repco won the championship again and became the first driver to win the Formula One World Championship in a car that carried his own name. In 1967 the title went to his teammate Denny Hulme.  Following injuries in the 1969 season Brabham intended to retire in 1970 but finding no top drivers available he raced for one more year, retiring after the Mexican Grand Prix. After retiring he made a complete break from racing, selling his interest in the team to Tauranac and returning to Australia. He was knighted in 1979.
All three of Brabham's sons - Geoff, Gary and David - are also engaged in racing careers.