The 40-1 shot, ridden by Padraig Beggy, flew from the rear of the field to edge Cliffs of Moher and favorite Cracksman in a race of changing fortunes.
Renowned trainer Aidan O'Brien now has six winners to his name in the past 17 runnings -- just one off the all-time record -- but few expected Wings of Eagles to emerge victorious.
The three-year-old colt, son of 2011 Derby winner Pour Moi, is the biggest priced winner of the Derby since Snow Knight (50-1) in 1974.
"When you're riding for Aidan O'brien you don't worry about the price," Begg told broadcaster ITV. "They always have a chance!
"I don't get to sit on too many beasts like this at the races so I'm going to enjoy it."
It was the jockey's first ever ride, and the O'brien pairing of Douglas Macarthur and The Anvil had looked the more likely in the early stages, opening up a three-length lead.
They were reined in by the bookie's favorites as the race approached the closing stages, with Ryan Moore's Cliffs Of Moher (5-1) and Frankie Dettori's Cracksman (7-2) striding ahead.
But with just two horses behind him with three furlongs to run, Beggy defied the odds to burst through the center.
"Paddy Beggy is a brilliant rider" enthused winning trainer O'Brien. "He's strong, he's got a great mind and is tactically very aware.
"What can I say? An absolutely world class rider. I can't tell you how delighted we are to have him working with us. I couldn't be happier"
It's a result that means Wings of Eagles joins the ranks of Galileo (2001), High Chaparral (2002), Camelot (2012), Ruler of the World (2013), and Australia (2014) -- all O'Brien winners.
It's a win that puts Beggy in the Derby history books.
"I'd probably given up on the big days," he said. "But Aidan O'Brien, bless him, has made it happen."