Because the C5-R had already proven itself a race-winning platform, Pratt Miller approached the C6.R as an evolution rather than a clean-sheet design. The simultaneous development of the road car and race car allowed engineering solutions to flow in both directions: features beneficial on the race car could be adapted to production models, and the C6.R was consequently able to carry more exotic design elements while still meeting homologation requirements. The exterior styling was aligned with the Corvette Z06 performance variant.
The C6.R retained the C5-R's Katech-built 7.0-litre V8, now more closely related to the production LS7 unit from the Z06. In its GT1 form the engine produced around 590 horsepower; unrestricted, Pratt Miller estimated output near 800 horsepower. The engine was recognised with the Global Motorsports Engine of the Year award in 2006. Chassis improvements included greater use of weight-saving aluminium, improved airflow via a redesigned front grille, and the permanent headlamp integration already introduced on the road car. A rear-facing camera feeding a cockpit monitor addressed the absence of a rear window, as did an air conditioning system for driver comfort.
One notable innovation introduced during the 2007 season was variable cylinder displacement — deactivating half the cylinders under caution conditions to reduce fuel consumption. The system encountered problems at the 2007 Le Mans and was withdrawn for further development. A separate GT2 variant, subsequently reclassified GTE, was launched in 2009 with a downsized 5.5-litre V8 producing approximately 470 horsepower, lighter aluminium frame, steel brakes, and aerodynamic styling borrowed from the Corvette ZR1 road car.
Corvette Racing debuted the C6.R in the full 2005 American Le Mans Series season. The newly entered Prodrive Aston Martin DBR9 won at Sebring, ending Corvette's run of consecutive victories stretching back to 2003. However, Prodrive returned to Europe after Sebring, and the C6.Rs won every subsequent ALMS round that season. At Le Mans, the team outlasted the quicker Aston Martins to take a 1-2 in GT1 and finish fifth and sixth overall.
The Aston Martin rivalry intensified in 2006. Corvette Racing avenged the Sebring defeat, and a close season-long points battle was resolved in Corvette's favour by a three-point margin in the final race — a second consecutive championship. At Le Mans, the Aston Martins faltered with reliability problems after leading, allowing a C6.R to win the GT1 class. The distance covered by Corvette Racing in taking that win set a record for homologated GT cars that remained unbroken as of 2022.
With Prodrive concentrating on Le Mans preparation for 2007, Corvette Racing had no significant ALMS opposition in GT1, winning nine of twelve rounds for a third championship. At Le Mans, the Aston Martins finally proved reliable enough over 24 hours and won, leaving Corvette Racing second. A third C6.R was entered at Mosport in tribute to Canadian driver Ron Fellows, painted in Canadian national colours matching a limited-edition road car.
The factory GT1 cars were retired after Le Mans 2009, having cumulatively demonstrated sustained superiority over the class's most competitive era.
The GT2 C6.R was introduced in mid-2009, immediately proving competitive — Jan Magnussen and Johnny O'Connell took second in the car's debut race at Mid-Ohio and won at Mosport. For 2011, Corvette Racing added a paddle-shift transmission and won the GTE-Pro class at Le Mans. Privateer team Larbre Competition won GTE-Am at Le Mans in 2011 and repeated the result in 2012. Corvette Racing won the 2012 and 2013 ALMS GT class titles before the C6.R was superseded by the C7.R for the 2014 season.
Several C6.Rs entered private hands within months of the factory cars' debut. GLPK-Carsport fielded a former factory car in the 2006 FIA GT Championship, winning at Paul Ricard and finishing third at the Spa 24 Hours. Carsport Holland, successor to GLPK-Carsport's Dutch arm, won the Spa 24 Hours in 2007, defeating the Vitaphone Racing Maserati. The Selleslagh Racing Team, the original C5-R customer, continued with a C6.R in Belgian and French championship competition. Luc Alphand Aventures earned factory support from Pratt Miller for a European campaign, winning the 2008 Le Mans Series teams and drivers championships.
The C6.R is widely regarded as one of the defining GT racing cars of the 2000s. Its rivalry with the Aston Martin DBR9 elevated both programs and produced some of the most compelling GT racing of the decade. The car's dual-configuration career — spanning the GT1 era under ALMS and FIA GT rules and then the GTE era under ACO and IMSA regulations — demonstrated an unusually broad competitive lifespan. Its technical platform directly underpinned the development of the C7 road car, completing the engineering feedback loop established when the C5-R was created.