The first road races in Bridgehampton were held on public roads around the hamlet of Bridgehampton from 1915 until 1921. The course ran counterclockwise on an approximately 3-mile (4.8-km) rectangle, beginning on Montauk Highway, then turning left onto Halsey Lane, left onto Pauls Lane, left onto Ocean Boulevard, and left back onto Montauk Highway.
The races were revived in 1949, utilizing a 4-mile (6.4-km) circuit adjacent to the pre-war circuit in Bridgehampton and Sagaponack. It ran clockwise beginning on Ocean Road, turning right onto Sagaponack Road, right onto Sagaponack Main Street, right onto Bridge Lane, and right back onto Ocean Road. The races proved successful, and joined the SCCA National Sports Car Championship when it was created in 1951. The road races came to an end in 1953, after a driver was killed in practice and three spectators injured during the race. These events, combined with a spectator death in a crash at Watkins Glen in 1952, led the State of New York to ban racing on public roads.
Local racing enthusiasts formed the Bridgehampton Road Races Corporation in 1953 to finance the construction of a permanent race circuit in the area. The corporation purchased a 550-acre (2.2 km2) parcel known as Noyack Hills in 1956, and constructed a 2.85-mile (4.59 km), 13-turn road course. Although construction was not completed, the first races were held in 1957. The headline event, the Bridgehampton Sports Car Races, were a part of the SCCA National Championship; Regional races would be added in 1958. The race would shift to the professional United States Road Racing Championship in 1965, and resurrected the Vanderbilt Cup, which had been run on Long Island from 1904 until 1910. A second National event was added in 1961. This event would shift to the World Sportscar Championship for 1962, marking Bridgehampton's biggest event. The WSC gave way to Can-Am from 1966 until 1969. Can-Am was scheduled to return in 1970, but the race was moved to the newly opened Road Atlanta after heavy storms damaged the track. A 1971 IMSA GT Championship event was the last major event at the track.
Bridgehampton's facilities remained primitive. Only a small media and scoring building and a small grandstand were installed. The Bridgehampton Road Races Corporation did not have the money to upgrade and maintain the tracks infrastructure to world-class standards. The track's land had appreciated to several million dollars in a few decades. Locals began complaining about noise in the mid-1970s, and in 1983 the town passed an ordinance limiting noise and effectively ending any chance of big-league racing returning. Plans were announced in 1994 to turn the property into a golf course. Races continued until 1997, and a racing school and club meets lingered until 1998.