Development of the C6.R was an evolution of the C5-R design, aided by the simultaneous development of the C6 generation Corvette road car. This allowed for the adaptation of design elements between race and road versions, facilitating homologation and enabling the C6.R to use more exotic features. The C6.R retained much of the framework and 7.0 litre V8 engine from the C5-R, though the engine was more closely based on the LS7 from the Z06, becoming known as the LS7.R, and earning the Global Motorsports Engine of the Year award in 2006.
Innovations included a video camera in the rear bumper with a monitor in the cockpit to compensate for the lack of a rear window, and an air conditioning system to improve driver comfort. A variable displacement system was tested in 2007 to improve fuel economy during caution periods, but was later removed due to failures. By the end of 2007, seven C6.Rs had been built, including one chassis adapted with C6.R bodywork but retaining a C5-R chassis, used as a show car.
Following the retirement of the C5-R at the end of 2004, the factory Corvette Racing squad began 2005 with two new C6.Rs, competing in the full American Le Mans Series season. After a loss at Sebring to Prodrive Aston Martin, Corvette Racing won the remaining races of the season, and achieved a 1–2 finish at the 24 Hours of Le Mans.
In 2006, Corvette Racing and Prodrive battled throughout the American Le Mans Series, with Corvette Racing winning the championship by three points. At Le Mans, Corvette Racing finished fourth overall and won the GT1 class. The Aston Martin - Corvette duel at Le Mans saw both rivals finishing with a record-breaking pace for homologated GT cars, with the distance record set by Corvette Racing unbroken as of 2022.
After Prodrive returned to Europe in 2007, Corvette Racing was the only competitor in the GT1 class for nine out of twelve races in the American Le Mans Series, easily winning their third championship. At Le Mans, Aston Martin won the GT1 class, leaving Corvette Racing in second place.
Corvette Racing entered a third C6.R at the 2008 Grand Prix of Mosport, painted in a special livery honoring Canadian driver Ron Fellows. In 2009, Corvette Racing transitioned to the GT2 class with a newly designed C6.R for the second half of the season.
In 2012, two C6.Rs competed in the LMGTE Pro category at the 24 Hours of Le Mans, with one car finishing 23rd overall. Corvette Racing won the 2012 GT Team's and Driver's championship with 4 class wins. They also won the 2013 ALMS GT championships with 5 GT victories, including the 12 Hours of Sebring.
Like the C5-R, used C6.Rs were sold to privateer teams once replaced by newer chassis. GLPK-Carsport, formed by a merger of PK Carsport and Carsport Holland, purchased a C6.R in 2005 and achieved a victory at Paul Ricard and a third-place finish at the Spa 24 Hours in the FIA GT Championship.
Carsport Holland won the Spa 24 Hours in 2007, and scored another victory at Nogaro before closing the season third in the drivers' championship. PK Carsport also returned to the C6.R chassis in 2009, winning the 24 Hours of Spa.
DKR Engineering ran a C6.R in the FFSA French GT Championship and the Le Mans Series, winning at Lédenon and finishing third at the 1000 km of Spa in 2006. They also competed in the FIA GT Championship and the 24 Hours of Le Mans.
Luc Alphand Aventures purchased a C6.R in 2007, receiving support from Pratt Miller. They won the Le Mans Series Team and Drivers Championship in 2008.
Selleslagh Racing Team, the first customer Corvette team, won several Belcar Championships and achieved a victory at Monza in the FIA GT Championship in 2008.
Larbre Competition won the GTE-Am class at the 2011 and 2012 24 Hours of Le Mans with a C6.R GT2.
In 2008, Corvette Racing announced a transition to the GT2 class for the 2009 American Le Mans Series season. The C6.R GT2 used a 6.0L V8 engine producing 470 bhp, based on the 7.0L LS7.R from the GT1 car. The engine was later downsized to 5.5L to comply with new regulations. The GT2 car featured an aluminum frame, smaller front splitter and rear wing, and steel brakes.
The new GT2 car achieved a second-place finish at Mid-Ohio and a win at Mosport in 2009. At the 2010 24 Hours of Le Mans, factory GT2 Corvettes retired due to engine problems and a collision. The car was upgraded with a paddle-shift transmission for the 2011 season, winning the GTE-Pro class at the 24 Hours of Le Mans. In 2012, the C6.R GT2 was widened to improve stability and mechanical grip, winning the 2012 ALMS GT championship.
Pratt Miller also produced the C6RS, a conversion of the Corvette Z06 that resembled the C6.R and shared components with the race car, producing 600 horsepower. Only seven C6RS cars were ever built.