Self-proclaimed "Universe Boss" Gayle bossed the England bowlers around once he hit his stride, smashing 12 sixes as he led West Indies to their highest score against England.
Playing his first ODI since the home series against Bangladesh last July and having announced that the upcoming World Cup will be his worldwide farewell in the format, the hard-hitting Windies star also helped set a new world record.
But, remarkably, it was not almost enough as Roy reached three figures off 35 fewer balls than Gayle and then Joe Root led England home and became the fastest Englishman to reach 5,000 one-day runs with the third and perhaps best century of the game.
Root, the Test captain who finally came good with a hundred in the last innings of the three-match series in St Lucia just over a week earlier, also got to three figures against the University of the West Indies Vice-Chancellor's XI last Sunday and tapped into that rich vein of form once more.
Shai Hope joined in the fun, with a six off Moeen Ali landing on the roof of the five storey media centre.
It still took time for Gayle to warm up as he had made only 21 after facing 50 balls and went to his 50 off 76.
Although it was an excellent wicket for batting, West Indies in particular were sloppy in the field, with Roy and Root both dropped twice.
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Bishoo was unlucky not to have Roy's wicket a few times in a new spell with Pooran and Bravo dropping chances.
The 39-year-old, who skipped his side's ODIs in India and Bangladesh before Christmas, was dropped on nine by Jason Roy and made England pay as he completed a 100-ball ton and 24th in the format, celebrating the milestone by taking off his helmet and balancing it on his bat handle.
Stokes eventually got the breakthrough when Hope, on 64, got a leading edge to third man.
Eoin Morgan contributed 65 runs off 51 deliveries before spooning Thomas to Holder at mid-off and, with Root and Ben Stokes at the crease, England needed 36 runs off 36 balls.
Root was denied hitting the winning run when he was caught on the boundary with the scores tied and left to a standing ovation. But then he went into overdrive, his first six taking him past Shahid Afridi with a record 477 global maximums, as ball after ball disappeared over the Oval's stands.
Hope - who had already overtaken Gayle after coming in at No. 3 - hit a enormous straight six off Moeen which landed on the roof of the media centre, some five storeys high.
However, the top-ranked ODI team, who will go into the World Cup as one of the favourites to lift the coveted title, fought back well over the final ten overs when it looked as if the home side would get closer to the 400-run mark with Gayle in full flow.