The Windies slumped to 164 for seven against New Zealand in pursuit of a target of 292 at Old Trafford, but that merely set the stage for Brathwaite, who bludgeoned nine fours and five sixes in a staggering 80-ball hundred.
However, with six needed for victory, Brathwaite swung mightily again, only to hole out to long-on, where Trent Boult held on to the catch and avoided stepping over the boundary as the Kiwis escaped with a five-run win.
Following his supreme 101, Brathwaite said: "Everyone believed that we could get over the line. It's obviously bittersweet. I know it's probably cliche to say the hundred doesn't matter if you don't win.
"But for me personally, for my confidence, I guess as a result of all the hard work I've been putting in, it's finally good that it's come to fruition.
"I'll continue to work hard, obviously devastated not to get over the line, but also I give thanks for the performance and even getting the team into a position that we got into before I got out.
"It's heartbreaking to get so close and not get over the line, but there were some positives and I think that the fight that the lower order showed was commendable.
"I thought I had enough bat on (the delivery that got him out). I was just willing it to go up and up and up.
"Unfortunately it didn't, they probably had one of the better fielders in the world down there. It is what it is. One or two yards more we'd have been victorious."
The Windies suffered a fourth consecutive defeat and, in all likelihood, their hopes of reaching the knockout stages are all but over as the Kiwis moved to the top of the standings.
Kane Williamson's sublime 148 from 154 balls had taken them to 291 for eight on a challenging surface, with a 160-run partnership alongside Ross Taylor (69 off 95) forming the bedrock of their innings.
Some mighty blows from Chris Gayle, in an 84-ball 87, and Shimron Hetmyer, who hit 54 from 45 deliveries, kept the Windies up with the run-rate, but Boult's four for 30 undermined their pursuit.
The Black Caps did not count on Brathwaite's tour de force display, but Boult had the final say.
He said of his catch: "It was a pressure situation, I guess. Initially I thought it was going to be quite a way inside the rope, but almost driven for six in the end, but nice to snaffle it.
"And what a game. Simple as that, really."
Scraping past the Windies in Manchester follows narrow wins over Bangladesh and South Africa, with Boult sure those on the other side of the world are enjoying following their fortunes.
He added: "It's a bit special. It's been a bit of an emotional roller coaster sitting there with the pads at times and then being under the pump there with the ball.
"It's what it's all about. It's awesome to be a part of it. And I'm sure there will be a lot of proud Kiwis back home, diving into poached eggs, watching a result like that."
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