The Target Chip Ganassi driver held off Will Power — who moved into the championship lead — to capture his second IndyCar win of the season.
"I've got to give a lot of credit to Team Target," said Dixon, who won the Honda Indy 200 last month. "They gave me a great car with great pit stops and great fuel strategy."
Team Penske's Power moved into first place in the standings with 542 points, 11 ahead of Dario Franchitti, who finished in eight place after being penalized for hitting Ryan Briscoe's car on the 26th lap.
Dixon, who finished 3.4375 seconds ahead of Power, is 59 points out of first place with two races to go. The final two races of the season in Kentucky and Las Vegas are on ovals.
Toronto's James Hinchcliffe finished 15th.
The deadly March 11 earthquake damaged the oval at Twin Ring, so Sunday's 63-lap race was held instead on the recently repaved 14-turn, 2.9-mile road course.
Franchitti's chances to hold onto his lead in the overall standings were damaged when he made contact with the right-rear of Ryan Briscoe's Team Penske car entering Turn 1 on the 26th lap.
Race officials levied an avoidable contact penalty on the reigning series champion, which sent him to the rear of the field. He advanced 17 spots to finish eight.
Dixon has the distinction of winning on both the oval and now the road course at Motegi, having taken out the 2009 race.
Danica Patrick, who started 23rd on the grid, moved up to finish in 11th place. Defending Indy Japan champion Helio Castroneves finished 22nd.
Sunday's race was the last IndyCar series event in Japan. Mobilityland Corp., a wholly owned unit of Honda Motor Co., announced in February that due to the global economic downturn the 2011 race will be the last.