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Dixon finished third at the season-ending Grand Prix of St Petersburg in Florida to finish 16 points clear of championship rival Josef Newgarden, who won the final race.
The 40-year-old knew he had to finish ninth or better to seal the series title.
"I never doubted it, never doubted it, not with you guys," Dixon said shortly after crossing the finish line.
"What a team! Thank you all so much boys and girls everybody. Well done, well done. This is all you guys thank you."
His sixth championship was built on his fast start to the season.
He won the first three races of the year and won again in race eight, but then fell short of the podium in the next five races before today.
Newgarden had whittled down Dixon's championship lead from 117 points to send the championship to a finale.
"I seemed to sleep fine. I don't know what everyone was worried about," Dixon joked.
"It definitely got pretty close there. Credit to Josef and Team Penske. They drove the last part of the season flawlessly and so many points so it was pretty awesome to race them again."
It is Dixon's second championship in three years to go with the titles he won in 2003, 2008, 2013 and 2015.
His six titles are one shy of the American open wheel record held by AJ Foyt.
"Six is good, seven sounds better. That's obviously going to be the goal but it's tough."
Fellow countryman Scott McLaughlin crashed out less than halfway through his IndyCar debut.
But McLaughlin was far from disheartened with the experience.
"It was awesome! Far out. It was the best day of my life apart from my wedding."
Speaking about the crash, he added: "It was going really well and I tried to block Marco, and I thought I was there or thereabouts but had half a rear-lock.
"The cold tyres put me off a bit. I'm really disappointed but I had a lot of fun today."