"What a great car, what a great team," Castroneves said. "What can I say? I am speechless. I want to thank our team and my teammates because we are working so hard together.
"We have been close so many times and finally luck was a little bit on our side.
"It is like I am winning for the first time."
He becomes the ninth different race winner of the year.
JR Hildebrand grabbed second place ahead of Ryan Hunter-Reay.
Castroneves has never won an IndyCars championship but brings himself right into the frame with this win.
Dixon had to make the best of a bad day and spent it in damage control.
"It kinda was," the 36-year-old said. "We really struggled the NTT Data car we were just so loose especially on the re-starts. About 25-30 laps into the run we could beat up the front right a little bit and then carry some speed but we could only run the high lines because as soon as we got on the bottom I would almost spin out.
"Trying to pass traffic was really tough.
"It was a fun race. Physically very difficult I thought just because our car was so neutral I was fighting it all day."
There are six races left in the series with the next round in Toronto next week.
Championship Standings
Scott Dixon 403 points
Helio Castroneves -8
Simon Pagenaud -31
Will Power - 53
Josef Newgarden -56
Graham Rahal -66
Takuma Sato -66
Tony Kanaan -108