After starting the final round in a six-way tie for second, two shots behind American Alex Smalley, Rai closed with a steely and at-times spectacular five-under-par 65 to post a landmark three-stroke triumph over Spanish star Jon Rahm and American Alex Smalley.
The 31-year-old is the first Englishman to hoist the Wanamaker Trophy since Jim Barnes won for a second time way back in 1919.
And Rai saluted in style, rallying back from three shots behind before making eagle at the par-5 ninth and all but sealing victory with a magical 68-foot birdie putt on the penultimate hole.
Rai had jostled for the lead all day as heavyweights Jon Rahm, Rory McIlroy, Xander Schauffele and Australia's resurgent former British Open champion Cameron Smith all duelled down the stretch.
He burst clear of the pack with five back-nine birdies, with Rahm (68) and Smalley (70) sharing the runner-up spoils.
After sitting anxiously on the clubhouse lead for more than four hours, two-time PGA Championship winner Justin Thomas had to settle for a share of third, four shots behind Rai, following a blazing final-round 65.
Rai's maiden major victory comes after just one previous win on the PGA Tour, at the 2024 Wyndham Championship. Â
But the breakthrough had been coming, with the world No.44 making the cut in his previous eight straight majors having featured on the weekend only once before that run.
After missing the cut at six majors in a row, Smith emerged from the golfing wilderness with a tie for seventh at four under alongside McIlroy (69) and Schauffele (69).
The 2022 British Open champion had a series of chances to grab a share of the lead but couldn't find a birdie on the back nine en route to a closing 68.