A 79th-minute penalty goal from replacement halfback Ryan Lonergan earned the Brumbies the lead for the first time on Friday night after the Blues had earlier threatened to run away with the match.
Despite winning 23 of their past 24 games against Australian opposition, the Blues couldn't deny the Brumbies a spirited comeback triumph on this occasion.
The hosts led 20-10 at the break after two runaway tries in the space of two minutes just before halftime to prop Angus Ta'avao and superstar centre Rieko Ioane.
Their lead would have been far larger had Beauden Barrett not sprayed two conversion attempts and a routine shot at a penalty goal.
But the Brumbies fought back doggedly in the second half, with a penalty goal from Declan Meredith reducing the deficit to seven points before the scrumhalf crossed out wide for his side's second try of the night.
Meredith missed the conversion attempt to leave the Brumbies trailing by two.
After dominating the scrum, lineout and breakdown, the Brumbies secured a decisive penalty with less than two minutes left, allowing Lonergan - lining up from in front 30 metres out - to boot them to a famous victory.
"It's really special," said Brumbies captain Allan Alaalatoa.
"We knew that it was going to take a special effort from everyone today and I thought that we delivered that.
"In the first half we were doing really well, especially in and around the ruck.
"They probably scored a few easy tries but that's what you get with quality backs.
"So the boys had to dig deep and it took 80 minutes and, yeah, I'm just really proud of the effort."
The match had been all locked up at 10-all through 35 minutes, after prop Alalatoa's pick-and-drive effort cancelled out Barrett's early strike for the Blues.
But Ioane's first try since May 2023, and his milestone 50th in Super Rugby, looked to have given the Blues all the momentum entering the second half.
The Brumbies, though, had other ideas, even if Lonergan felt like a bundle of nerves lining up the match-winning shot at goal as the clock wound down.
"Pretty nerve-wracking, to be honest," he said of his clutch play.
"We worked so hard throughout the whole game. The forwards knew they were in for a massive day against a quality Blues pack and the least I could do was kick it over."
The loss avenged a 34-20 season-ending semi-final defeat to the Blues last year.
Alaalatoa hopes the breakthrough win at New Zealand's traditional rugby stronghold can spark the Brumbies to another title run.
"But we've also got to understand what put us in this position to win the game," he said.
"Look at our preparation and what worked for us and just continue to build on that.
"We've got a really tough game at home next Friday against the Fijian Drua so we've got to make sure the boys get home safe and we'll prepare for that."
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