A 79th-minute penalty goal from 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'avo 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 to boot the Canberrans to a famous victory.
The match had been all locked up at 10-all through 35 minutes, after Brumbies captain Allan 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.