The American golfer - who was paired by the world number one, his countryman Scottie Scheffler - held off Sam Burns by one shot to claim victory but he had to deal with a hostile home audience at Shinnecock Hills, who frequently shouted "get in the bunker" and failed to offer much in the way of cheering for his good shots.
Wyndham's victory came a year after he was banned by Oakmont Country Club, who hosted last year's US Open, after damaging a locker in frustration at his performance.
Speaking after his victory, he said: "New York didn't really like me. I love you guys, but, you know, I get it.
"Some of it is self-deserved. I did some unfortunate things last year that I really regret.
"I've been sorry multiple times and I'm still sorry, so hopefully I can win you guys over eventually.
"But I get it, they root for Scottie. Grand Slams only happen a few times. He's going to get it. He's the best player in the world, but today it's my day."
Scottie, who was chasing the Grand Slam, admitted some of the crowd's conduct was "a bit much" but praised Wyndham for sealing victory in the face of such a "tough" audience.
He said: "The crowd was tough today. New Yorkers, they are tough people.
"There was a good turnout from the fans. You like seeing the fans cheer for you. I think sometimes it can get a little too much when balls are kind of going off greens and you start hearing cheers. That felt a bit much to me.
"But, at the end of the day, I can't control fan behaviour. Being in the arena is not for everybody. There's been crowds that have been for me in my career; there's been crowds that have been significantly against me in my career.
"I think Portrush was a scenario for me where Rory (McIlroy) is in his hometown. Or not his hometown; he's in Ireland, not far from where he grew up. Crowds can be tough.
"Being in the arena is not for everybody, and I think it shows a lot about Wyndham, how he handled not only this golf course, but I think the crowd today as well and is a well-deserving champion.