The first races in Watkins Glen were organised by Cameron Argetsinger, whose family had a summer home in the area. With Chamber of Commerce approval and SCCA sanction, the first Watkins Glen Grand Prix took place in 1948 on a 6.600-mile course over local public roads. For the first few years races passed through the heart of the town with spectators lining the sidewalks. After a car driven by Fred Wacker left the road in the 1952 race, killing seven-year-old Frank Fazzari and injuring several others, the race was moved to a wooded hilltop southwest of town. The 1948–1952 street course is listed in the New York State Register and National Register of Historic Places.
A second public-road layout of 4.600 miles began use in 1953. The first permanent course — the Watkins Glen Grand Prix Race Course — was constructed on 550 acres and designed by Bill Milliken and Cornell University engineering professors. This 2.350-mile layout, used from 1956 to 1970, became the foundation of the modern circuit.
In 1961, just six weeks before the scheduled date, Cameron Argetsinger was tasked with preparing Watkins Glen to host the final round of the Formula One World Championship. Innes Ireland won the 1961 United States Grand Prix in a Lotus-Climax, launching an autumnal tradition that drew huge crowds and became one of the most popular events on the global Grand Prix calendar. The race received the Grand Prix Drivers' Association award for best organised and best staged Grand Prix of the season in 1965, 1970, and 1972.
Before the 1971 race, the circuit underwent its most significant transformation: the layout was extended from 2.35 miles to 3.377 miles by the addition of a curling, downhill section through the woods known as "The Boot" or "Anvil." The pits and start-finish line were moved to a new pit straight, and the circuit was widened and resurfaced. In 1975, a fast right-left chicane was added to the Esses section following the fatal crashes of Francois Cevert in 1973 and Helmut Koinigg in 1974; this "Scheckter Chicane" was later removed in 1985.
The Formula One race was ultimately removed from the schedule in May 1981 after the circuit failed to pay its $800,000 debt to the teams, ending two decades of Grand Prix racing at the Glen.
Without Formula One the circuit struggled financially and declared bankruptcy in 1981. In 1983, Corning Enterprises and International Speedway Corporation purchased the track and renamed it Watkins Glen International. The renovated circuit reopened in 1984 with the return of IMSA. NASCAR's top series returned in 1986 on the short 1971 Six Hours layout.
The most recent structural change to the course came in 1992, following a series of serious crashes at the Loop at the end of the back straight. A bus stop chicane was added, dubbed the "Inner Loop," which slightly lengthened both layouts. This came weeks after NASCAR Cup driver J. D. McDuffie died at the same site during the 1991 Budweiser at The Glen.
Two distinct configurations are in current use. The Boot layout (long course) measures 3.4 miles and incorporates the full downhill Boot section used by the IndyCar Series and IMSA. The 1971 Six Hours course (short course) is used by NASCAR and bypasses the Boot complex. Both share the modified Inner Loop chicane added in 1992. The entire circuit was repaved in 2015.
International Speedway Corporation became the sole owner in 1997; the facility is now owned by NASCAR. IndyCar racing returned to Watkins Glen in 2016 after a five-year absence.
The 1973 Summer Jam concert drew an estimated 600,000 fans to the facility featuring The Allman Brothers Band, the Grateful Dead, and The Band. Phish held festivals at the site in 2011 and 2015. The annual Zippo U.S. Vintage Grand Prix is considered one of the nation's premier historic racing events.
Watkins Glen International is one of the headline American road courses on iRacing, featured across multiple series ranging from the NASCAR iRacing Series to sports car and open-wheel championships. Both the Boot and Short Course layouts are typically available, letting sim racers experience the dramatic elevation change through the Boot section and the technical Inner Loop complex that have defined circuit strategy for decades.