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Whyte, who has been WBC interim champion for over a 1,000 days, hoped victory over Povetkin would finally land him his long-sought-after shot at the world title.
The 32-year-old Brit star came out strong against the veteran Povetkin as he took control of the bout in the early stages.
Whyte made the breakthrough against the 40-year-old Russian star when he knocked him down twice in the fourth round.
But Povetkin then did the unthinkable in the fifth as he connected with a clean left uppercut to send the 'Body Snatcher' crashing to the canvas.
Povetkin's victory at Matchroom Headquarters has now put him in line to face the winner of Tyson Fury vs Deontay Wilder for the WBC championship.
Speaking after the fight, the newly crowned interim WBC champ claimed that he felt "confident" even after he was knocked down twice in the fourth.
Povetkin told Sky Sports: "I didn't feel I would finish [the] fight like this. I was confident in the fourth round even after going down twice."
The Russian boxer went on to say that he had studied Whyte's previous fights and exploited his vulnerability of missing uppercuts from the left and right.
"I was watching his fights and taking into account he was missing uppercuts from the left and right," Povetkin explained.
Fury, who won the WBC title in February after his masterclass performance against Wilder, took to Twitter to congratulate Povetkin on his victory.
Whyte's promoter, Eddie Hearn, has confirmed that the Brit does have the option to activate a rematch clause with Povetkin.
The 41-year-old Matchroom chief told Sky Sports: "When the punch landed, I thought it was a dream. I can't believe it.
"Two heavy knockdowns from Whyte -- people felt it was over. This is the drama of heavyweight boxing. One punch completely changed the fight. I felt confident Whyte would end the fight.
"It is a shock. He wasn't that much of an outsider -- we knew how good Povetkin was. It was a thrilling knockout on a thrilling night.
"We have a rematch clause. Dillian said, 'Give me a rematch, give me rematch.' We will exercise that clause -- and have it before the end of the year.
"We know Povetkin won't be the immediate mandatory, so that frees up Tyson Fury to fight Anthony Joshua if he beats Wilder."
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