Hunter-Reay crossed the timing line in 1 minute, 17.6277 seconds to earn his first pole of the season and deny Dixon the top starting spot. Dixon, who is vying for a fifth IndyCar title, went 1:17.7599 and was atop the leaderboard until the very end when Hunter-Reay moved ahead of him.
Dixon has a 29-point lead over Alexander Rossi in the standings and the pole would have given him an additional point before Sunday's race. The event is worth double points and Rossi, a teammate of Hunter-Reay's at Andretti Autosport, will start sixth.
"I'm certainly doing my part, I just took a point away from Dixon," said Hunter-Reay, who earned the seventh pole of his career and first since Long Beach in 2014.
On Sunday, though, Hunter-Reay will be out for himself.
"I'm just focusing on winning the race," he said. "That's all I can focus on, that's all I can do. I'll race like I always do, go for a win. That's our only objective. That's my only objective. That's the only reason why I'm here."
Rossi has lagged behind Dixon in every practice and qualifying session at Sonoma, and his team is trying to play strategy in their favor. He gambled on tire selection for the final round of qualifying and felt it backfired.
"We tried something a little different in hopes it would pay off, did the Firestone blacks for the Fast Six. But at the end of the day it clearly is probably not the right decision," Rossi said. "At this point we're trying to hit some home runs and get it done. It wasn't meant to be."
Reigning champion Josef Newgarden qualified third and was followed by Marco Andretti and Patricio O'Ward, who qualified fifth for his IndyCar debut. A nine-time winner in Indy Lights this season, the Mexican advanced into the Fast Six round in his Harding Racing entry.
Will Power had a rare off day in qualifying and wound up seventh, out of contention to challenge for an eighth pole this season. It's Power's lowest starting position of the season.