The oval was the only purpose-built competitive racing oval in Japan. It was a low-banked, egg-shaped course with turns three and four being significantly tighter than turns one and two. CART held the inaugural Indy Japan 300 at Twin Ring Motegi on March 28, 1998, won by Mexican driver Adrian Fernandez. CART continued racing there from 1998 through 2002, after which Honda entered the Indy Racing League and the race transferred to the IRL schedule as the Indy Japan 300.
The oval gained additional international attention in 2008 when Danica Patrick became the first woman to win an IndyCar race at Motegi, defeating Helio Castroneves. The 2011 IndyCar season was the last at Motegi, with the oval having sustained damage from the 2011 Tohoku earthquake; that year's race was relocated to the road course. The oval subsequently fell out of use for competitive racing and was periodically used as additional parking during MotoGP events, while still serving Honda's annual Thanks Day event showcasing road and racing vehicles from the adjacent Honda Collection Hall. The circuit also hosted a single NASCAR exhibition race in 1998, won by Mike Skinner — notable for being the first oval NASCAR race in Japan and the first event in which Dale Earnhardt and his son Dale Earnhardt Jr. competed against each other.
The road course is 4.801 km long and runs clockwise, the opposite direction from the oval. Although it shares garage and grandstand facilities with the oval, the two circuits are entirely separate — and race operations cannot occur simultaneously on both because teams must cross the road course pit lane and front straight to access the oval. The road course is built in a stop-start straight-and-hairpin style and is exceptionally flat by Japanese standards, with only a slight elevation rise toward its hairpin. Three configurations are possible: the full course plus two shorter layouts using connecting roadways, typically used for junior formula events such as Formula 4.
The road course's most prominent event is the Japanese motorcycle Grand Prix, which has been held there annually since 2004, having previously hosted the Pacific motorcycle Grand Prix from 2000 to 2003. The venue also hosts rounds of the Super Formula Championship and Super GT series each year, along with numerous domestic Japanese racing series. Access to the circuit presents a logistical challenge: the facility is served by only two entry and exit points on a two-lane public road, train links to the area are extremely limited, and accommodation near the track is scarce aside from the on-site hotel. The stated spectator capacity of approximately 65,000 is dictated primarily by traffic flow rather than physical seating capacity.
Beyond the two main racing circuits, Mobility Resort Motegi operates a second road course known as the North Short Course for karting and Formula 4 events, a 0.402 km dirt track for modified and sprint car racing, and an outdoor trials course that hosts the FIM Trials World Championship annually. The Honda Collection Hall on site displays historic Honda road and racing vehicles and motorcycles. Honda Fan Fun Lab presents next-generation Honda technologies including robotics, fuel-cell vehicles, and aviation. A technology demonstration center and educational facilities also operate within the complex.
As a modern, large-scale Japanese circuit built in 1997 with Honda's backing, Motegi has achieved wide representation in motorsport simulation and gaming, appearing in titles such as Gran Turismo 4, Gran Turismo 5, Gran Turismo 6, Forza Motorsport 2, Forza Motorsport 3, Forza Motorsport 4, iRacing, and RaceRoom Racing Experience. The circuit was also featured in Honda's 2005 Clio Awards-winning commercial "Impossible Dream," in which a BAR Formula One car was driven into the bridge on site.