The Texas-raised "Lonestar J.R." is one of nine drivers to win the prestigious Indianapolis 500 mile race at least three times: in 1974, 1976, and 1980. The others are Louis Meyer, Wilbur Shaw, Mauri Rose (credited with only two by official speedway records), A. J. Foyt, Al Unser, Bobby Unser, Rick Mears and Hélio Castroneves. Rutherford also won three poles at the 500, in the years 1973, 1976, and 1980. He retired from racing before the start of the 1994 Indianapolis 500 and now serves as an official with the Indy Racing League, driving the pace car for all IRL races, except the ceremonial pace car during the start of the Indianapolis 500.
Rutherford also dabbled in stock car racing, making 35 NASCAR Winston Cup starts from 1963 to 1988. Rutherford won in his first start, at Daytona International Speedway driving for Smokey Yunick. The win, in the second 100-mile Daytona 500 qualifying race, made him one of the youngest drivers ever to win in NASCAR history, in a full points-paying NASCAR race. (Until 1971, the qualifying races were full points-paying races.) In 1981, Rutherford drove twelve races, the most he ever raced in a single NASCAR season. In addition, Rutherford competed in five runnings of the International Race of Champions - 1975, 1977, 1978, 1980, and 1984.
Johnny Rutherford was the Honorary Chairman of the Amelia Island Concours d'Elegance in 2006.