Having established the C5-R as a proven race winner, Pratt Miller approached the C6.R as an evolution rather than a clean-sheet design. A key advantage in development was that, unlike the C5-R which debuted years after the C5 generation road car, the C6.R and the sixth-generation Corvette were developed simultaneously. This allowed racing-derived features to inform the road car and vice versa, with the C6.R sharing its exterior styling with the Corvette Z06.
Much of the mechanical framework of the road C6 was retained, along with increased use of weight-saving aluminium. The move away from the C5's pop-up headlamps to fixed units integrated into the bodywork improved aerodynamic flow over the front of the car. The large front grille opening served to channel air simultaneously to the brake cooling ducts and to generate aerodynamic benefit.
Beneath the bodywork, the C6.R retained a Katech-built 7.0-litre V8 engine, now more closely based on the road car's LS7 unit. This engine, designated the LS7.R, received the Global Motorsports Engine of the Year award in 2006 for its performance and endurance qualities. In unrestricted form it was capable of approximately 800 hp. The car also featured an in-cockpit video monitor fed by a rear bumper camera, providing drivers with better rearward visibility in the absence of a rear window — an innovation carried over and refined from the C5-R era.
One significant technical development introduced during the 2007 season was a variable displacement system that disabled half of the engine's cylinders during caution periods to reduce fuel consumption. Although tested in competition, a failure at the 2007 24 Hours of Le Mans led the team to remove it from the cars pending further evaluation.
Six C6.Rs were built by Pratt Miller by the end of the 2007 season. A seventh vehicle, built on a C5-R chassis with C6.R bodywork, was used as a development and show car and never competed.
Corvette Racing debuted the C6.R in the 2005 American Le Mans Series with two cars. The season opened against the new Prodrive Aston Martin DBR9, which won the opening round at Sebring. After Prodrive returned to Europe, the C6.Rs won every remaining round. When Prodrive returned for the final two events, the Corvettes extended their streak and took both races. At the 24 Hours of Le Mans, the C6.Rs outlasted the faster DBR9s to claim a 1-2 finish in the GT1 class, finishing fifth and sixth overall.
In 2006, Prodrive concentrated on the American Le Mans Series, creating a closely fought season-long duel. Corvette Racing won the championship by a three-point margin in the final race. At Le Mans that year, the Aston Martins again suffered reliability problems after leading, allowing a C6.R to finish fourth overall and win the GT1 class. The pace set by both cars at Le Mans 2006 established a new distance record for homologated GT cars that remained unbroken as of 2022.
Prodrive's return to European racing in 2007 left Corvette Racing without a major GT1 opponent in the American Le Mans Series, and they were the sole competitors in the GT1 class for nine of twelve rounds, securing a third consecutive championship. At Le Mans, Aston Martin finally maintained their pace reliably over 24 hours to claim the GT1 class victory, leaving Corvette in second.
Corvette Racing ran the GT1 C6.Rs in the early races of the 2009 American Le Mans Series season and retired them from GT1 competition following the 24 Hours of Le Mans, redirecting their factory effort to a newly developed GT2 car.
The C6.R GT2, announced in September 2008, used a newly designed 6.0-litre V8 producing 470 hp. For the 2010 season this engine was further reduced to 5.5 litres to comply with updated GT regulations, though this displacement penalty required the team to carry additional weight concessions compared to competitors such as the Ferrari F430 GTC. The GT2 car used an aluminium frame rather than the steel frame of the GT1 car, incorporated smaller aerodynamic elements, and used steel rather than carbon ceramic brakes.
The GT2 programme achieved significant results: the C6.R won the GTE-Pro class at the 24 Hours of Le Mans in 2011 after receiving a paddle-shift transmission for that season. The car also took the 2011 American Le Mans Series GT class title and repeated the championship in 2013 with five class victories including the 12 Hours of Sebring.
Former factory C6.R GT1 chassis were sold to privateer teams relatively quickly — within a year of their factory debut, faster than the C5-R era. Notable privateer operations included GLPK-Carsport and Carsport Holland in the FIA GT Championship (Carsport Holland won the Spa 24 Hours in 2007), Luc Alphand Aventures in the Le Mans Series, and Belgian squad Selleslagh Racing Team in multiple European championships. Larbre Compétition successfully campaigned the GT2 variant in FIA World Endurance Championship GTE-Am competition, winning that class at the 24 Hours of Le Mans in both 2011 and 2012.
The C6.R GT1 and its GT2 derivative formed the backbone of Corvette Racing's factory programme from 2005 through to the introduction of the C7.R in 2014, representing the longest-running single platform in the factory Corvette Racing effort up to that point. Its dual-class success — winning in GT1 from 2005 to 2010 and in GTE-Pro and GT from 2009 to 2013 — demonstrated the longevity of the Pratt Miller engineering approach. A character loosely inspired by the car, Jeff Gorvette, appeared in the 2011 Pixar film Cars 2.