Collins won nearly 75% of her first-serve points while claiming three of her seven break points on her way to victory in just over two hours after a stunning final set that left the crowd, including former Miami champion Andre Agassi breathless.
"This is my first WTA 1000 and I worked so hard, it has taken me a bit longer than a lot of the other players," Collins told Sky Sports.
"This whole week has been tough - I have played against some of the best players in the world, including being out here and sharing the court with Elena in the final.
"Thank you to the fans. I've played a lot of tennis and in a few finals, but nothing compares close to this."
Collins, who said in January she would retire from tennis at the end of the season, was the surprise winner at the East Coast tournament, going one step further than her performance at the 2022 Australian Open when she reached the final.
She joins Martina Navratilova, Chris Evert, three-time champion Venus Williams, eight-time winner Serena Williams and Sloane Stephens as the sixth American woman to claim the crown.
The unseeded American relied on her strength to hold the lead at the start, converting break points against Rybakina, who kept levelling the score, before closing out the opening set with a stunning cross-court backhand winner on the hour mark.
Rybakina refused to go quietly after her opponent took a 2-0 lead in the second set and worked her way back, capitalising on unforced errors to draw level at 3-3.
However, the American regained the advantage after saving three break points to take the seventh game with the former Wimbledon champion unable to recover.
Rybakina, who lost last year's Miami final to Petra Kvitova, missed Indian Wells this month with a gastrointestinal problem.
She returned to the courts and put in a superb run, beating Belarusian Victoria Azarenka in three sets in the semi-finals, but admitted she did not expect to fight for the title.
"We didn't expect coming here to be in the final, to be honest, but it was a great two weeks. A lot of tough matches and great battles," she said.
