In March 1840, the first races were held on Saltwater Flat on the banks of the Maribyrnong River. The Port Phillip Turf Club took a lease of the site but, in 1852, was replaced by the Victoria Turf Club, which organised the first Melbourne Cup in 1861. The Victoria Jockey Club had appeared in 1857, and the two rival clubs amalgamated in 1864 to form the Victoria Racing Club (VRC). R.C. Bagot was appointed secretary, followed by Henry Byron Moore in 1881. An Act of Parliament gave the VRC legal control of the site in 1871, allowing it to make by-laws relating to racing there that, in turn, became applicable to racing generally.
Gradually a racecourse took shape. In 1861 a railway connected the racecourse to Spencer Street, and a new grandstand was built in 1873. Rose gardens and lawns were laid out and spaces designated: the betting ring, the birdcage, and the mounting yard enclosure. Flemington became a favourite with the public: the Hill opposite the finishing post; the Flat in the middle of the course with a small admission fee from 1913; and on the opposite side of the Maribyrnong River, Scotchmans Hill, which, while not as desirable, was free. When a new members' stand was built in 1925, it offered a more discrete space, but was situated well back from the finishing post. This tradition has been maintained: in 1978 the four-tiered public Hill Stand was completed, still positioned opposite the finishing post.
In other ways Flemington was conservative. It was not until 1931 that a totalisator was installed. This gave women direct access to gambling facilities, but in 1946 a white line in the members' stand was introduced, restricting women's access to certain areas. It was not until 1982 that women became entitled to be full members and the white line was lifted.
Apart from the Melbourne Cup, Flemington hosts other major races: the Victoria Derby (1855), the Oaks (1861), the Australian Cup (1863) and the Grand National Steeplechase (1866). The reconstruction of the racecourse has recognised its historical tradition in a large mural by Harold Freedman, in the 1990 restoration of Carbine's original stall, and in statues of Phar Lap and Bart Cummings.