In the 101st running of the iconic US auto race in the midwestern state of Indiana, Sato passed three-time victor Helio Castroneves of Brazil in the closing laps of the 200-lap drive around the oval track, and held on to win by the slim margin of two-tenths of a second.
The only driver to lead more laps was Chip Ganassi's Chilton, who lead the race after the final restart, but was powerless to keep Sato, Castroneves and Jones from passing.
Sato's win marked Andretti's second consecutive win as Alexander Rossi made it first to the finish line previous year.
Although Fernando Alonso didn't win the Indianapolis 500 on Sunday, he most likely won himself some new fans stateside. Always I invite 100, 150 kids from the devastated area, and we do a go-karting event.
"I had a few hours" sleep, so I had a headache and was kind of feeling not great", he said, "and oh, my gosh, was it just a dream? It was a tough, tough race.
"I'm really happy for Honda".
"It was fantastic race".
Sato said he didn't know he would win the race with three laps remaining running side-by-side with Castroneves.
Yet as a race team owner, Michael Andretti is now dominant. I believe him. We (went) side-by-side in Turn 1.
They had come to us and said, 'We can give you a little less reliable engine, but it will have more power.' We all, of course said, 'Let's go for the power'. I won two times there, I won two World Championships.
"I can't begin to thank the Japanese fans", he said. Hunter-Reay's Honda blew on Lap 137, when he was running in second place.
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"We kept pushing on, kept making up positions", the 23-year-old from Dubai said. "We pitted just before the last caution which put us back up front".
Honda ended the race with one flawless story, a Japanese driver winning in one of its own cars, but the stature and fame of Alonso means its association with his repeated frustrations will resonate just as much as Sato's victory in the motorsport world and beyond. After Alonso's engine troubles, it didn't take long for another yellow flag period, brought out by an accident that involved Power, Josef Newgarden and James Hinchcliff.
Rookie Ed Jones then made a courageous move on Castroneves to tuck in behind Chilton.
Sato passed three-time victor Helio Castroneves in the waning laps and held on to win, laying the ghost of a heartbreak at "The Brickyard" in 2012. Sato later made his move on Chilton and overtook the Briton on the outside.
In a Chevrolet for Team Penske, Castroneves briefly took the lead but couldn't hold it as Sato grabbed it back.
The race was red-flagged on Lap 55 for a frightening crash on Lap 53 when Jay Howard got out of the groove in Turn 2, hit the outside retaining wall coming down the track and collected pole-sitter Scott Dixon. Dixon and Howard both climbed from their cars.
While it didn't end the way Alonso hoped, seeing his number atop the famous scoring pylon at Indianapolis Motor Speedway was a thrill he won't forget.
"It was definitely a bit of a rough ride", Dixon said, typically understated.
"I had to make a decision on which way to go", he said of the incident. "I would have gone into the wall".
"Again, I will say I'm sorry, I know better and I'm angry at myself because there was no constructive objective in saying it." he added.
Winning the 500 would have been magical for Alonso, a two-time Formula One champion racing at Indianapolis for the first time.
"Thanks to IndyCar, unbelievable experience", he continued. "I had to believe in myself and what the auto was capable of".