The road course had been designed internally by IMS in 1992, with the redesign of the Brickyard Crossing golf course taking the future layout into account. The impetus for construction came when IMS president Tony George arranged in 1998 for Formula One to return to the United States for the first time since 1991. A two-year renovation and construction project followed, adding the infield road course alongside new pit garages and a new Pagoda building housing race control and the media center. The circuit was completed in 2000, and the inaugural United States Grand Prix at Indianapolis was held that year with over 200,000 spectators in attendance, among the largest crowds in Formula One history.
The standard road course measures 2.605 miles (4.192 km) and features the full front straight of the oval, the southwest banked turn, and an infield section. Modifications approved by the FIA and FIM extended the layout to a total of 16 turns for motorcycle racing. For MotoGP, the course was designed to run counter-clockwise — the same direction as oval events — and the banking of oval turn one was bypassed by a new infield section called the Snake Pit Complex. The double-hairpin after the Hulman Straight was also replaced with traditional esses. In 2008 and again in 2014, the road course layout was further modified to accommodate motorcycle racing and to improve competition.
Beginning in 2014, the IndyCar Series began using the road course for its IndyCar Grand Prix, held in early May as a lead-in to the Indianapolis 500. The infield section was modified once again at that point to make the circuit more competitive for open-wheel cars.
The United States Grand Prix at Indianapolis ran from 2000 to 2007. The inaugural race in 2000 was widely celebrated as a success and played a pivotal role in Michael Schumacher's 2000 World Championship campaign. However, the event's brief history was marked by controversy. The 2002 United States Grand Prix ended in a staged-looking photo finish between teammates Michael Schumacher and Rubens Barrichello, which drew widespread criticism. The 2002 race was also the first Formula One event to feature SAFER barriers.
The most damaging controversy came in 2005, when Michelin determined their tires were unsuitable for the banked oval section after two heavy crashes in practice involving Ralf Schumacher. At the last moment, the Michelin-supplied teams withdrew from the race, leaving only the six Bridgestone-shod cars to compete. The spectacle prompted mass walkouts, costly ticket refunds, and lasting reputational damage. The race returned for two further seasons but attendance and interest declined, and it was dropped from the calendar after 2007. Formula One moved its United States Grand Prix to the Circuit of the Americas in Austin beginning in 2012.
From 2008 to 2015, the speedway hosted a round of Grand Prix motorcycle racing, the first motorcycle events at the facility since 1909. The counter-clockwise motorcycle layout, with its Snake Pit Complex infield additions and revised hairpin section, gave the course a distinct character from its car-racing configuration. Motorcycle racing returned to the venue via the MotoAmerica Championship of Indianapolis beginning in 2019.
From 2014 onward, the IndyCar Series held its IndyCar Grand Prix on the road course each May as a companion event to the Indianapolis 500. The combination of road-course racing one week before the oval's premier event gave the speedway two distinct spectacles across its consecutive weekends. The road course was modified in 2014 to better suit IndyCar machinery, improving overtaking opportunities.
The road course also hosted NASCAR events. In 2020, the Pennzoil 250 Xfinity Series race was moved to the infield road course, and in 2021 the Cup Series race followed with the Verizon 200, replacing the traditional Brickyard 400 oval race for that year.
The Indianapolis Motor Speedway Road Course demonstrated that America's most iconic oval could sustain a second identity as a purpose-grade road racing venue. Its ability to host Formula One, MotoGP, IndyCar, and NASCAR on the same asphalt — each with tailored layout modifications — reflects the adaptability built into its original design. The circuit sits within a National Historic Landmark, making it one of the few FIA Grade One facilities to carry that designation.