After winning six national karting championships in the World Karting Association, Hunter-Reay won a Skip Barber Karting Scholarship to race in the Skip Barber Formula Dodge Series in 1999, winning the series championship. He then won a shootout against Formula Dodge drivers for the Skip Barber Big Scholarship and its $250,000 prize.
Hunter-Reay first competed in the Barber Dodge Pro Series in 1998, driving the No. 28 Reynard 98E-Dodge V6 without sponsorship. He started and finished 23rd on debut at Mid-Ohio Sports Car Course after contact with John McCaig on lap 22. In 2000, as winner of the Barber Dodge "Big Scholarship" Shootout, he drove the No. 31 Reynard 98E-Dodge V6, achieving a best finish of second at Nazareth Speedway and finishing fifth in the standings with 104 points. He also won the Barber Dodge Pro Series Rookie of the Year award. In 2001, Hunter-Reay won his first race in the series at Lime Rock Park, leading 21 of 30 laps, and took a second win at Exhibition Place after passing Matt Plumb in the closing laps.
In 2002, Hunter-Reay competed in the Toyota Atlantic Championship, then the main development series for the FedEx CART Championship Series, driving the No. 1 Medlock Ames Winery/U.S. Print Swift 014.a-Toyota 4A-GE for Hylton Motorsports. He won three races — at Laguna Seca Raceway, Chicago Motor Speedway, and Burke Lakefront Airport — finishing sixth in the standings with 102 points.
Hunter-Reay entered the Champ Car World Series in 2003 driving the No. 31 American Spirit Team Johansson Reynard 02i-Ford Cosworth XFE for American Spirit Team Johansson, a team owned by former Formula One and Champ Car driver Stefan Johansson. The team competed for most of the season without sponsorship. Hunter-Reay scored his first Champ Car win at the season-ending Lexmark Indy 300 at Surfers Paradise Street Circuit, leading for fifteen laps while others crashed on a drying track.
In 2004 he drove for Herdez Competition in the No. 4 Herdez Lola B02/00-Ford Cosworth XFE, winning at the Milwaukee Mile by leading all 250 laps and finishing ninth in the championship with 199 points. In 2005, with Rocketsports Racing, Hunter-Reay was replaced by Michael McDowell for the final two races after starting fifteenth and finishing tenth at Las Vegas Motor Speedway.
Hunter-Reay joined Rahal Letterman Racing for the final six races of the 2007 season as replacement for Jeff Simmons, finishing 19th in points with 119 points and winning the series Rookie of the Year award — setting the record for fewest starts in a season by a winner of the award. In 2008, at the Indianapolis 500, Hunter-Reay qualified twentieth after crashing on Pole Day but finished sixth and won the race's Rookie of the Year award. He took his first IndyCar Series win at the Camping World Indy Grand Prix at the Glen at Watkins Glen International, leading on a lap 52 restart ahead of Ryan Briscoe, Scott Dixon, and Darren Manning, giving Rahal Letterman their first win in four years.
In 2009, without a full-time team after American Ethanol withdrew sponsorship, Hunter-Reay drove the No. 21 Vision Racing Dallara IR07-Ilmor-Indy V8 HI7R and delivered Vision their best result with a second place at the season-opening Honda Grand Prix of St. Petersburg. At the Indianapolis 500 he was bumped by John Andretti but requalified by 0.0324 seconds over Alex Tagliani, then crashed on lap 20. He later replaced injured Vítor Meira at A. J. Foyt Enterprises, scoring a fourth at Mid-Ohio.
In 2010, Hunter-Reay drove for Andretti Autosport, initially part-time. He led 64 of 85 laps to win the Toyota Grand Prix of Long Beach on the Streets of Long Beach. At the Indianapolis 500, on lap 199 in turn three, he ran out of fuel, causing Mike Conway to drive over the left side of his car and flip into the catch fence. He finished the season seventh in points with 445 points.
In 2011, at the Indianapolis 500, Hunter-Reay was bumped from the field by teammate Marco Andretti with 55 seconds remaining in qualifying. Andretti then made a deal for Hunter-Reay to replace Bruno Junqueira in an A. J. Foyt Enterprises car, from which he started 33rd. At the MoveThatBlock.com Indy 225 at New Hampshire Motor Speedway, he led for 71 laps before rain caused IndyCar officials to revert results to lap 215.
In 2012, driving the No. 28 DHL/Sun Drop Dallara DW12-Ilmor-Chevrolet Indy V6 — named after Dan Wheldon, who had tested the car at Mid-Ohio and Indianapolis Motor Speedway — Hunter-Reay won three consecutive races at the Milwaukee IndyFest at the Milwaukee Mile, the Iowa Corn Indy 250 at Iowa Speedway, and the Honda Indy Toronto at Exhibition Place, then added a fourth win at the Grand Prix of Baltimore. At the season-ending MAVTV 500 IndyCar World Championships at Auto Club Speedway, both he and Will Power received 10-grid penalties for exceeding the five-engine limit. Power spun on lap 56; with Power in 25th, Hunter-Reay needed a top-five. Tony Kanaan crashed on lap 241. On the final lap, fourth-place Takuma Sato spun and Hunter-Reay avoided him to finish fourth, winning both the overall championship with 468 points and the oval championship with 168 points. He became the first American to win the series championship since Sam Hornish Jr. in 2006.
In 2013, driving the No. 1 DHL/Sun Drop Dallara DW12 as defending champion — the first to use number 1 since Scott Dixon in 2004 — Hunter-Reay won twice, at Barber and Milwaukee, finishing seventh in points with 469 points. For 2014, driving the No. 28 DHL Dallara DW12-Honda Indy Turbo V6, he qualified a disappointing nineteenth for the Indianapolis 500 but won the race by 0.0600 seconds over Helio Castroneves, the second-closest finish in Indianapolis 500 history behind 1992. He finished sixth in the final standings with 563 points.
Over the six seasons from 2015 through 2020, Hunter-Reay recorded only five wins and none since Sonoma in 2018, while younger Andretti Autosport drivers Alexander Rossi and Colton Herta emerged as team leads. On August 18, 2021, he announced he was leaving Andretti Autosport for a sabbatical from full-time IndyCar competition, returning for the Indianapolis 500 and select events with Dreyer & Reinbold Racing.
Hunter-Reay sat out the 2022 IndyCar Series but provided development and insights for Juncos Hollinger Racing and rookie Callum Ilott ahead of the 106th Indianapolis 500. In 2023, he ran the 107th Indianapolis 500 with Dreyer & Reinbold Racing, finishing eleventh, then replaced the released Conor Daly at Ed Carpenter Racing for the remainder of the season before being let go at year's end to make way for 2023 Indy NXT Champion Christian Rasmussen. In 2024, Hunter-Reay drove the 108th Indianapolis 500 again for Dreyer & Reinbold with Cusick Motorsports.
Hunter-Reay made his American Le Mans Series debut in 2002 at the Mobil 1 12 Hours of Sebring for JMB Racing in the No. 31 Ferrari 360 Modena-Ferrari 3.6 L V8 with Peter Argetsinger and Andrea Montermini in the GT class, retiring after 28 laps. He returned to the series in 2010 with Level 5 Motorsports in the LMPC class. In 2011, co-driving the No. 055 Lola B11/40-HPD HR28TT with Scott Tucker and Luis Díaz, he won the LMP2 class at the 12 Hours of Sebring, finishing 20th overall.
In the Rolex Grand-Am Sports Car Series, Hunter-Reay co-drove with Jim Matthews, Marc Goossens, and Jimmie Johnson at the 2007 Rolex 24 at Daytona. That year he also co-won the Discount Tire Sunchaser 1000 at Miller Motorsports Park. At the 2013 Rolex 24 at Daytona, driving for VelocityWW in the No. 10 Velocity Worldwide Dallara Corvette DP-Chevrolet with Max Angelelli and Jordan Taylor, the car finished second overall after leading for 56 laps and completing 709 laps.
In the IMSA Tudor United SportsCar Championship in 2014, driving for SRT Motorsports in the No. 91 SRT Viper GTS-R-SRT 8.0 L V10 in GTLM, Hunter-Reay co-drove with Dominik Farnbacher and Marc Goossens, qualifying on class pole at the Rolex 24 at Daytona and finishing third in class.
During the 2006–07 A1 Grand Prix season, Hunter-Reay represented the United States alongside Phil Giebler and Jonathan Summerton for A1 Team USA, entered by West Surrey Racing, driving a Lola B05/52-Zytek V8. He made his debut at Taupo Motorsport Park in New Zealand, finishing eleventh in the sprint race and tenth in the feature race.
In 2012, Hunter-Reay competed in the Race of Champions as the sole IndyCar Series representative, the first since Bertrand Baguette in 2010. He formed the Americas team with Benito Guerra Jr. In individual competition he faced Tom Kristensen in Volkswagen Sciroccos, David Coulthard in KTM X-Bows, Romain Grosjean in Audi R8 LMSes, Kazuya Oshima, and Michael Schumacher in Euro Racecars. He returned in 2014, partnering with Kurt Busch, who had been his teammate at Andretti Autosport for the 2014 Indianapolis 500.
Hunter-Reay is married to Beccy Gordon, former Champ Car World Series pit reporter and off-road racing driver, and the sister of Robby Gordon. He has three children and resides in Fort Lauderdale, Florida. He owns a Yellowfin Yachts 42-foot yacht named Inside Line. Hunter-Reay appeared in the NBC Sports Network television series IndyCar 36 with an episode covering his race weekend at the 2012 Toyota Grand Prix of Long Beach. A documentary titled Ryan Hunter-Reay: An American Champion, following Hunter-Reay, his wife Beccy, and newborn son Ryden in the months after his 2012 championship win, was also broadcast on NBC Sports Network.
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