DRR entered the Indy Racing League in 2000 and won its debut race at Walt Disney World Speedway, where Robbie Buhl drove from the 22nd starting position to take the victory. The team was one of the few to run consistently on Infiniti engines until the manufacturer departed the series, subsequently switching to Chevrolet and then to Honda in 2005.
In 2002, the team fielded a second car for Sarah Fisher. At Kentucky Speedway that season, Fisher became the first woman in North American motorsports history to win the pole position for a major-league open-wheel race. In the 2006 Indianapolis 500, the team's second entry was piloted by Al Unser Jr.
When Buhl retired from the cockpit in 2004, the team placed Felipe Giaffone in the car, followed by Roger Yasukawa. With Honda backing gone for 2006, Buddy Lazier became the primary driver. Ryan Briscoe showed strong pace in wet conditions at Watkins Glen International that year to claim a podium, one of the team's better results of the period.
For 2007, DRR recruited two former Fernandez Racing engineers and named Buddy Rice and Sarah Fisher as its drivers. Rice delivered a solid season, finishing ninth in the championship with three top-five results. Fisher struggled to place seventeenth in points, often given equipment inferior to the team's first car, and announced her departure in late 2007 citing a lack of commitment from DRR.
Rice returned in 2008, with the team's second car shared by Milka Duno and Townsend Bell. Both Rice and Bell finished inside the top ten at the Indianapolis 500, placing eighth and tenth respectively, while Duno finished nineteenth. The 2009 season brought a complete driver overhaul: British rookie Mike Conway joined as the full-time lead, with the second seat rotating between Darren Manning, Milka Duno, and Tomas Scheckter. Conway, along with John Andretti and Duno, all qualified on bump day for the 2009 Indianapolis 500. Conway showed road-course speed across the year, taking a podium finish in third at Infineon Raceway.
Justin Wilson joined DRR for the 2010 season in the No. 22 Z-Line Designs car. At the Toronto street circuit, Wilson posted a record lap time of 1:00.2710 seconds to take pole position in the Firestone Fast Six shootout, achieving it without using any of the faster alternate-compound tyres. He led much of the race but lost grip exiting turn 11 on a late restart and spun, eventually recovering to finish seventh. Following Conway's Indianapolis 500 injury, the team expanded to four entries at various points, with Tomas Scheckter, Graham Rahal, and Paul Tracy among those who raced for DRR. J. R. Hildebrand made his IndyCar debut with DRR at Mid-Ohio that year.
Conway departed for Andretti Autosport for 2011, replaced by rookie Ana Beatriz with sponsorship from Petroleo Ipiranga. Wilson remained for a second season, and the team also fielded Simon Pagenaud and Giorgio Pantano at various rounds.
In November 2011, DRR and Group Lotus announced that DRR would serve as a Lotus factory partner team for the 2012 IndyCar season, using the new Lotus IndyCar V-6 engine. Oriol Servia was named the full-time driver. In April 2012, the two parties mutually agreed to end the engine contract; in May, DRR announced a strategic alliance with Panther Racing, gaining access to a Chevrolet engine contract. Performance improved markedly, with back-to-back top-five finishes at Indianapolis and Detroit. Servia closed out the season with three further top-ten results, finishing thirteenth in the championship.
DRR and Panther continued their alliance for the 2013 season with Servia again driving, but the team withdrew from competition after the 2013 Indianapolis 500 due to loss of primary sponsorship. The decision did not affect Panther Racing's own programme.
From 2014, DRR returned as a part-time entry focused primarily on the Indianapolis 500, operating in partnership with Kingdom Racing. Sage Karam debuted for the team that year, starting 31st and finishing ninth. Townsend Bell ran the 2015 Indianapolis 500 for the team, finishing fourteenth. Karam appeared again in 2016 before crashing midway through the race. J. R. Hildebrand partnered Karam in 2018 and 2019; Hildebrand's eleventh-place finish in 2018 was the best result of the team's part-time era to that point.
In January 2020, DRR announced expansion to at least four races: St. Petersburg, the GMR Grand Prix, the Indianapolis 500, and Toronto. Karam drove all four, with Hildebrand returning for Indianapolis. Subsequent seasons saw Ryan Hunter-Reay, Conor Daly, Stefan Wilson, and Graham Rahal race for the team.
Dennis Reinbold, who had built and led the organisation since its founding, died in June 2026 after a battle with cancer.
DRR entered the Global RallyCross Championship in 2016, where Cabot Bigham won the GRC Lites championship. In 2017, Christian Brooks finished second and Travis PeCoy third in the junior class. The team switched to the Americas Rallycross Championship in 2018, where Brooks was the ARX2 runner-up.
In 2021, DRR signed a partnership with KYB EKS JC to compete in Nitro Rallycross. For the 2022–23 season, operating as Dreyer & Reinbold Racing JC in alliance with JC Raceteknik, the team expanded to a four-car programme in the Group E class. Robin Larsson won the driver's championship; teammates Andreas Bakkerud and Fraser McConnell finished second and third. DRR JC also won the team championship by a substantial margin. In the ARX2 class during 2021, Cole Keatts finished runner-up and Conner Martell third, while Sage Karam added a win and four runner-up finishes in a part-time entry.
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