Nicky Hayden, who has died following a cycling accident aged 35, was one of the greatest motorcycle racers of the modern era. He came from humble beginnings in Owensboro, Kentucky, to win the 2006 MotoGP world championship, defeating the reigning champion Valentino Rossi in an unforgettable final-race showdown.

Like most riders from the US, Hayden started out in dirt track, wrestling bikes around loosely surfaced oval circuits and learning the art of throttle control. It is no coincidence that many European racers, including Rossi and the reigning MotoGP champion Marc Márquez, now include this discipline in their training regimes.

But Hayden was slightly different. His entire family went racing: his father, Earl, mother, Rose, and siblings, Tommy, Jenny, Kathleen and Roger Lee. The family enjoyed its proudest moment when Nicky, Tommy and Roger Lee finished one-two-three at the Springfield Grand National in Illinois. Meanwhile Rose and his sisters competed in so called “powder-puff” dirt-track races. Hayden rode throughout his career with the number 69, which he inherited from Earl, who liked it because it read the same whether the bike was right way up or not.

Hayden’s dirt-track skills stood him in good stead when he graduated to racing on asphalt in the late 1990s. American Honda soon recognised his talent and signed the youngster, who won the 1999 600cc US Supersport championship and the 2002 1000cc US Superbike title.

Nicky Hayden at a press conference in Madonna di Campiglio, 2013, while riding for the Italian manufacturer Ducati. Photograph: Max Rossi/Reuters

That latter success propelled him into the premier MotoGP world championship, again riding for Honda, this time as team-mate to the young Rossi. Hayden had so much to learn during his early years on the global scene: new motorcycles, new racetracks, new rivals and a whole new way of life.

His dedication to his cause was outstanding. He worked very hard; always the last man out on track when his team went testing to fine-tune his motorcycles and develop new parts. He won his first MotoGP race in 2005 at his home event, the US Grand Prix at Laguna Seca, California.

The following year Hayden mounted his first challenge for the title. He won two more races, but still went into the season finale eight points down on Rossi, who had dominated the five previous championships. Few expected the newcomer to overcome that disadvantage, but Hayden always had remarkable self-belief. He defeated Rossi and won the crown, joining other American greats such as “King” Kenny Roberts, Kevin Schwantz and Wayne Rainey in the motorcycling pantheon.

Motorcycle racing is a tough sport, often dominated by riders who wear their egos on the outside. Hayden was polite and charming, with a winning smile, as well as a winning throttle hand. He was proud of his humble background. Earl owned a car dealership in Owensboro called Second Chance Autos. His son liked to say, “I don’t want y’all thinking it’s the kind of place where doctors and attorneys go buy their cars.”

Hayden endured several years in the doldrums after his 2006 title success. New technical regulations transformed MotoGP bikes from fire-breathing 990cc motorcycles into smaller, higher-revving 800cc machines. These bikes required a different riding technique that did not allow Hayden to exploit his skills so successfully.

In 2008 he left Honda to join the Italian manufacturer Ducati, which also had its difficulties staying competitive with the dominant Japanese manufacturers. Hayden scored a handful of top-three results aboard Ducati’s Desmosedici, but it was always obvious that he was riding to the limits of the bike. Lingering injuries caused him other problems. Finally in 2016 he left the MotoGP paddock to join the World Superbike series, again riding for Honda. Last year in Malaysia he won his first World Superbike race. This season he stayed with the same team and was lying 13th in the points standings.

Last week Hayden was cycling in Rimini, Italy, when he was in collision with a car. He suffered serious head injuries and never regained consciousness.

Hayden is survived by his fiancee, Jackie Marin, and by his parents and siblings.

• Nicholas Patrick Hayden, motorcycle racer, born 30 July 1981; died 22 May 2017