The Brumbies needed just a single point in Canberra to reach the playoffs for the first time since 2004 by securing the title and the position in the top three of the final standings that goes with it.
They were well beaten by the Blues, however, and the Reds later ran in five tries to beat the New South Wales Waratahs 32-16 in Brisbane.
That left the Brumbies, who have 58 points, hoping the Bulls or Sharks, who both have 54, slip up in their final matches against the Lions and Cheetahs respectively to clinch one of the two remaining playoff spots.
The Blues were already well out of contention after a hugely disappointing season but first-half tries from Liaki Moli, Daniel Braid and Hadleigh Parkes were enough to fire them to their fourth victory of the year.
"They'll be gutted about that result," Brumbies coach Jake White said in a televised interview.
"The reality is we let ourselves down with that performance in defence, which is something we've prided ourselves on this year.
"It's a tough lesson for us that it's not over until the fat lady sings."
The Brumbies did not help their cause by letting Auckland's backs run riot with a string of missed tackles and were kept in the game by a fine individual try from winger Henry Speight and the kicking of Zack Holmes and Jesse Mogg.
They could still qualify for next week's first round of the playoffs but the faltering manner of their progress, should they make it, will not strike fear into the hearts of their prospective opponents.
The Blues absolutely dominated the opening quarter of the match with lock Moli converting pressure into points by bulldozing over the line from close range after 11 minutes.
Six minutes later and flanker Braid crossed in the corner through a string of tacklers after centre Francis Saili had run back a clearance kick through the heart of the midfield. Piri Weepu converted both to give the Blues a 14-0 lead.
The first foray by the Brumbies into the visitors' half after 20 minutes produced a penalty that allowed Holmes to eat into the lead and three minutes later Speight danced down the right touchline to score his side's only try.
Holmes converted and added another penalty to cut the lead to just one point but Blues winger Parkes took advantage of some more loose tackling to stretch the lead once again, and another Weepu conversion saw them turn around 21-13 ahead.
Mogg cut the lead by three points with his only succesfull kick from four penalty attempts six minutes after the break but two Weepu three-pointers extended the lead to 11 points.
The Brumbies knew that defeat by seven points or less would secure them a bonus point and the title but Holmes missed his third attempt at goal in the 59th minute.
With the rain now pouring down on Canberra Stadium, Blues' replacement back Michael Hobbes put the final nail in the coffin with a final penalty two minutes from time.
"I'm so proud of them," said Blues coach Pat Lam, who was delayed joining his team in Australia after having had to undergo an interview for his own job.
"It's been a really tough season, we've had so much crap thrown at us."