Agostini was born in Brescia, Lombardy, and grew up in Lovere, where his father ran a transport company operating ferries on Lake Iseo. Racing against his father's wishes, he began competing in hill climb events before moving to road racing. At 21 he won the 1963 Italian 175cc championship on a Moto Morini, and in 1964 won the Italian 350cc title while scoring his first World Championship points with a fourth place at the West German Grand Prix.
Those results attracted Count Domenico Agusta, who signed Agostini in 1965 to ride alongside Mike Hailwood for the MV Agusta factory team. In his very first race for the squad he beat Hailwood to win the 350cc West German Grand Prix at the Nurburgring. A mechanical failure cost him the 1965 350cc title in the final round at Suzuka, handing it to Honda's Jim Redman.
When Hailwood departed for Honda in 1966, Agostini became MV Agusta's lead rider and claimed his first 500cc World Championship, becoming the first Italian 500cc champion since Libero Liberati in 1957. He also scored the first of his ten Isle of Man TT victories that year, winning the Junior TT.
The 1967 season produced one of the most dramatic championship battles in the sport's history. Agostini and Hailwood traded race wins throughout the year, their duel at the Isle of Man TT reaching a climax on the final lap when Agostini's roller chain broke while the two were locked together at the front. The title was not settled until the final round at Mosport, Canada: both riders finished with five victories each, but Agostini took the championship on the tiebreaker of second-place finishes — three to Hailwood's two. Despite their fierce competition, both men remained friends; after Hailwood died from injuries sustained in a 1981 traffic accident, Agostini served as a pallbearer at his funeral.
Honda's withdrawal from racing after 1967 left Agostini without serious factory opposition in the larger displacement classes for several seasons. From 1968 to 1970 he won every race he contested in both the 350cc and 500cc classes. His 1968 double — winning both the 350 and 500 World Championships — launched four consecutive doubles. By 1971 he had won 58 consecutive races across the two classes before a breakdown at the Junior TT ended the streak. That year he claimed his tenth World Championship, surpassing the previous record of nine shared by Carlo Ubbiali and Mike Hailwood.
When Agostini's close friend Gilberto Parlotti was killed in an accident during the 1972 Isle of Man TT, Agostini announced he would never again compete at the event, declaring the 37.73-mile public-road circuit unsafe for World Championship competition. His stature as the reigning champion gave the decision enormous weight in the sport. A wider walkout by top Grand Prix riders followed, and the FIM eventually withdrew the Isle of Man TT from the World Championship calendar after the 1976 races. Agostini maintained that he opposed only the contractual obligation for championship competitors to enter such a dangerous event, not the race itself.
By 1972 the competitive threat from two-stroke machinery was intensifying. Yamaha's Jarno Saarinen won three 350cc races and handed Agostini his first head-to-head defeat since the 1967 Canadian Grand Prix. Agostini successfully defended the 350cc title in 1972 and the 500cc title in 1973, but his new MV Agusta teammate Phil Read proved unwilling to play a supporting role and won the 1973 500cc championship after Agostini's early-season mechanical failures stripped him of points.
Frustrated by team politics and by MV Agusta's development stagnation following Count Agusta's death in 1971, Agostini signed a six-figure contract with the Yamaha factory for 1974 after ten years and 13 World Championships with MV Agusta. He proved his credentials on two-stroke machinery immediately, winning the 1974 Daytona 200 on the new Yamaha TZ750 against a field including Kenny Roberts and Gary Nixon, then winning the Imola 200 a month later. He won the 350cc title that year — the first time a two-stroke motorcycle had won the 350 class — despite a disrupted season of crashes and mechanical failures in the 500cc class.
In 1975 Agostini won his fifteenth and final World Championship in the 500cc class, again the first time a two-stroke motorcycle had claimed the premier class title. His seven consecutive 350cc World Championships came to an end when teenage prodigy Johnny Cecotto beat him to the title.
After Yamaha withdrew from racing following the 1975 oil crisis, Agostini ran his own Marlboro-backed team using MV Agusta machinery before acquiring a Suzuki RG500. In the wet 1976 West German Grand Prix at the Nurburgring he won on the MV Agusta — the final Grand Prix victory for both himself and the marque, and the last 500cc class win by a four-stroke motorcycle. He competed through 1977 without adding another Grand Prix win, then retired from motorcycle racing at 35.
Agostini subsequently attempted a career in car racing, contesting non-championship Formula One events in 1978, competing in European Formula 2 in a Chevron B42-BMW, and entering the British Aurora Formula One series before concluding his automotive career in 1980.
Agostini returned to motorcycle racing as team manager of the Marlboro Yamaha squad in 1982. Under his management, Eddie Lawson won three 500cc World Championships. He later managed the Cagiva factory team from 1992 until the manufacturer's withdrawal in 1994, and concluded his managerial career in 1995 with a 250cc Honda squad.
In 14 Grand Prix seasons, Agostini started 223 races, finished on the podium 159 times, and recorded 122 victories. His 15 World Championships and 122 Grand Prix wins remain the all-time records in Grand Prix motorcycle racing. He won the Senior Isle of Man TT five consecutive times from 1968 to 1972 and the Junior TT five times between 1967 and 1972.
Agostini was inducted into the AMA Motorcycle Hall of Fame in 1999, the MotoGP Hall of Fame in 2000, and was named an FIM Legend in 2010. A section of road on the Isle of Man TT circuit at Quarterbridge Road is named "Ago's Leap" in recognition of a famous photograph capturing him lofting the front wheel of his motorcycle over the crest.
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