The 30-year-old Collins, number 53 in the world, is the lowest-ranked woman ever to win the tournament, clinching her biggest career title in a two-hour triumph, as per AFP.
Collins announced in January that she will be retiring from the sport at the end of this year and her unexpected run to the final and victory over the world number four delighted the home crowd.
"I couldn't think of a better way to win my first 1000 title. It means the world to me," Collins said.
"The encouragement and support that I got, it was hard to hide the emotion because I think these are the moments that we live for and we don't always get to have them. It was really special," she said.
While she insists that her recent run of form won't lead her to reconsider her departure from the sport, Collins will rise to 22 in Monday's WTA rankings.
It was a disappointing second straight loss in a Miami final for Rybakina, who missed out to Petra Kvitova last year.
Both players looked strong on their serve in the early exchanges but Floridan Collins had to work hardest to hold her serve.
She saved four break points as she hung on for 4-3 and showed resistance again to deny a break point at 5-5 with a brilliant backhand winner after a long rally.
Collins broke at the end of the first set, capitalizing on a third break point to win the set when Rybakina went long.
Then the momentum shifted heavily in Collins's direction when she broke Rybakina's first service game of the second set.
The 24-year-old Rybakina, the 2022 Wimbledon champion, responded, breaking back at the first opportunity.
Neither player was able to truly dominate, but Collins struck the decisive blow when she broke to go 5-3 up as Rybakina at full stretch on the baseline went long.
The American had not defeated a top five player since a win over then-world number two Paula Badosa at San Diego in October of 2022.
Perhaps it was inevitable then that Collins showed nerves at the end as she struggled to serve out, denying two break points and finally clinching on her fourth championship point.
"It's hard," Collins said. "You've got the crowd supporting you and pushing you to close it out and they wanted me to win so bad. It was like playing in front of my best friends and I didn't want to let the crowd down and it was tough.
"Elena does not give up and she just kept slinging those shots right and left, I just had to hang in there."
Rybakina had missed out on Indian Wells due to a gastrointestinal illness and said that with four of her five matches in Miami en route to the final having gone to three sets, she was not in peak condition.
"I was feeling the body, of course. Also, it was not [an[ easy tournament, because the first matches I was playing quite late, finishing, and then I was going to sleep around 2:00, 3:00. Then some matches were during the day. So the schedule was also up and down, and recovery, it doesn't help, for sure," she said.
"I had a lot of tough matches. Some of them went my way with a bit of luck here and there. This one didn't, and of course I was not expecting to be fresh in this final, and she played really well," she added.
Collins becomes the first American woman to take home the Miami Open title since Sloane Stephens in 2018 and the sixth overall, also joining Martina Navratilova, Chris Evert, three-time champion Venus Williams and eight-time champion Serena Williams.
The previous lowest-ranked women's champion was Kim Clijsters, who was ranked 38th when she won the title in 2005.