It is long known around the world as the former home of the Formula One United States Grand Prix, which it hosted for twenty consecutive years (1961–1980).

The Watkins Glen International racecourse has undergone several changes over time, with five general layouts widely recognized over its history.

The Watkins Glen Grand Prix Corporation was formed to manage spectators, parking, and concessions; this arrangement lasted three years.

At the end of the backstretch, after the Loop-Chute, cars swept left into a new four-turn complex that departed from the old layout, curling left-hand downhill through the woods.

The new layout measured 3.377 miles (5.435 km); with its intrinsic link to the Formula One race, it became known colloquially as the Grand Prix Circuit.

In 1973, French driver François Cevert, a previous winner at the Glen, died in a crash during practice at the 1973 United States Grand Prix.

This led course officials in 1975 to add a fast right-left chicane to slow speeds in the turn 3-4 Esses section.

In 1991, during the IMSA Camel Continental VIII, Tommy Kendall's Intrepid RM-1 prototype crashed in the Loop, severely injuring his legs.

Seven weeks later, NASCAR Winston Cup driver J. D. McDuffie died in an accident at the same site during the 1991 Budweiser at The Glen.

Having already won both Driver's and Constructor's World Championships and still mourning the death of Wolfgang von Trips at the 1961 Italian Grand Prix, Ferrari decided not to compete in the United States GP.

Hopkins was the most recognizable starter in Grand Prix racing, wearing a lavender suit, clenching a big cigar in his mouth, and giving the job everything he had.

Once the cars had taken their places, Hopkins strode across the front of the grid with his back to the field, turned, and jumped into the air while waving the national flag to start the race.

From 1968 through 1981, the "Six Hours at The Glen" endurance race featured top drivers such as Mario Andretti, Jacky Ickx, Pedro Rodríguez, and Derek Bell.

During the IMSA Camel Continental VIII, Tommy Kendall's prototype crashed in Turn 5, severely injuring his legs.

Seven weeks later, NASCAR Cup Series driver J. D. McDuffie died in an accident at the same site in the 1991 Budweiser at the Glen.

In 1997, International Speedway Corporation became the sole owner of the course, as Corning Enterprises believed they had completed their intended goals to rebuild the race track and increase tourism in the southern Finger Lakes region of New York State.

Grandstands from Pennsylvania's Nazareth Speedway, which had closed, were installed, the gravel in The 90 was removed and replaced with a paved runoff area, and curbing was cut down for the Indy Racing League event.

Augmenting what was already in place along the front stretch, additional high safety fences were installed on the overpasses crossing the service roads at the top of the esses and just out of the boot immediately after the exit of turn 9.

Officials installed a new control tower, which includes booths for the officials, timing and scoring, television and radio (the new position allows broadcasters to see more action from Turn 10 through the foot of the Esses), and the public address announcer on top of the new front stretch grandstand, moving the start-finish line farther ahead of the bridge, as the start-finish line is moved 380 feet (120 m) farther toward The 90 in order to accommodate the new timing and scoring post.

Race Services Inc. provides the track with volunteers to work Fire-Rescue, Medical, Grid personnel, and Corner workers to help keep drivers and spectators safe.

The track named the trophy for the inaugural Watkins Glen Indy Grand Prix presented by Argent in honor of the late patriarch, Cameron.

On Tuesday, March 6, 2007, just before 9 pm, a fire destroyed the recently remodeled Glen Club situated on top of the esses.

The loss included irreplaceable, unique original motorsport artwork donated to the facility by several artists and other racing memorabilia.

The NASCAR weekend at the Glen received a double shot—Zippo Manufacturing announced a three-year extension of the Busch-Nationwide Series race, the "Zippo 200".

Additionally, Brad Penn lubricants of Pennsylvania (former Kendall Oil refinery) was announced as the sponsor of the annual vintage sports car weekend for 2007 and 2008.

IndyCar took a six-year hiatus from the facility when the series pulled out of the Glen after 2010 due to a dispute with track owner ISC.

14 Mobil 1 Chevy for four laps around the circuit while Hamilton drove the MP4-23, Vodafone McLaren Mercedes's entry in the 2008 Formula One season.

Before this event, the curbs on some of the turns were changed, the white rumble strips being replaced by the more common, red-white designs seen on most road courses around the world.

It was held over the Labor Day weekend and used the full layout: ICS officials were also negotiating with WGI to race there permanently.

[12] As of August 2024, the fastest official race lap records at Watkins Glen International are listed as: * from minimum 10 starts.