He drove in the AAA and USACChampionship Car series, racing in the 1953-1960 seasons with 69 starts, including the Indianapolis 500 races in each season. He finished in the top ten 43 times, with 7 victories. His best Indy finish was third in 1959. Roy Sherman, the first National Midget Champion, was his chief mechanic for several Indy 500s.
He was the first driver to win a 100-mile (160 km) dirt track race in less than an hour at Langhorne, Pennsylvania. His champ car's average speed was 100.174 miles per hour.
The Indianapolis 500 was part of the FIA World Championship from 1950 through 1960. Drivers competing at Indy during those years were credited with World Championship points and participation. Johnny Thomson participated in 8 World Championship races. He started on the pole once, set 1 fastest lead lap, and finished on the podium once, accumulating a total of 10 World Championship points.