A win for Terry Butcher's side would have secured third place in the Clydesdale Bank Premier League and the final Europa League berth.
But Aaron Doran's opener was cancelled out by Ryan Dow, before Gary Mackay-Steven struck in injury time to hand United their first post-split win.
The result means the race for Europe goes to the wire, with Inverness, St Johnstone and Ross County still in contention as it stands ahead of County's game against Motherwell.
Butcher's men looked set to take the lead when referee Crawford Allan pointed to the spot after David Raven was felled in the box by John Rankin after 34 minutes.
Billy McKay stepped up for the spot-kick but, for the second week in a row, failed to convert from 12 yards when Radoslaw Cierzniak saved well, seconds after being booked for dissent.
However, the United goalkeeper was plucking the ball out of the back of the net three minutes before the break when Raven teed up the shot for Doran and he rifled into the back of the net from the edge of the area.
The visitors were back on level terms four minutes after the restart when Willo Flood's free-kick was nodded on for Dow to lash home his first SPL goal.
Inverness piled forward in search of the goal that could seal their place in Europe and Andrew Shinnie blazed a desperate attempt over from just inside the box.
A Nick Ross cut-back then found Doran in an ideal position but he ballooned his shot over the stand completely. Instead, they were hit with the sucker punch when United grabbed the winner in injury time when Mackay-Steven rifled home at the far post.
Aberdeen extended their unbeaten run under new manager Derek McInnes to four matches but their goalless draw at St Mirren was a largely forgettable way to mark the 30th anniversary of their greatest triumph.
Three decades ago to the day, Alex Ferguson's Aberdeen side beat Real Madrid in Gothenburg to win the European Cup Winners' Cup but the current team are proving less effective on their travels.
Aberdeen have still not won an away game in 2013 although they came closer to three points than their hosts with Jonny Hayes seeing a goal disallowed and Marc McAusland clearing off the line from Scott Vernon.
And they looked secure at the back despite the continued absence of Russell Anderson, claiming their third clean sheet under McInnes.
Both sides lined up with two strikers and two attack-minded wingers - Dougie Imrie and Gary Teale for the hosts and Niall McGinn and Jonny Hayes for the Dons.
But the formations did not translate into much meaningful goalmouth action from two teams that have struggled in recent months.
St Mirren have now gone 10 Clydesdale Bank Premier League games without victory, although they made four changes after the Dons secured their survival with a 1-1 draw at Dundee last weekend.
Jim Goodwin, Jon Robertson, Imrie and Sam Parkin came into the starting line-up with Kenny McLean suspended, Paul McGowan absent and both Steven Thompson and Lee Mair dropping to the bench.
Aberdeen were without suspended pair Rory Fallon, who was sent off at Dens Park, and Peter Pawlett, whose dive earned his side the crucial penalty and a two-match ban. Stephen Hughes dropped out with the fit-again Hayes coming in along with forwards Scott Vernon and Cammy Smith.
It took 17 minutes for either side to come close. Vernon curled just over the top corner from 18 yards after some excellent close control from Ryan Jack.
St Mirren threatened moments later when Jamie Langfield pushed over Dougie Imrie's dipping, swerving 30-yard free-kick.
Mark Reynolds did well to head clear as Parkin looked set to finish off a cross from Conor Newton, who soon forced a save from Langfield with a 20-yard drive.
The best chance of the half fell to Joe Shaughnessy when McGinn's corner found him eight yards out but the Aberdeen right-back's downward header was stopped by Saints goalkeeper Craig Samson.
Aberdeen created the best chance of the game just after the break.
Vernon had seen a turn and shot saved before Hayes set him up three yards out with a cross to the back post. The English striker looked certain to nod home but Marc McAusland got his head in the way to divert the effort wide.
Ryan Jack volleyed wide from another decent chance after Vernon's lay-off and Aberdeen had the ball in the net in the 69th minute.
Vernon held up a long ball and laid it off to the onrushing McGinn, who helped the ball on to Hayes. The Irishman tucked the ball into the far corner from 14 yards but the assistant referee had his flag raised and it looked the correct decision despite protests from the visitors.
That was the end of the action although there was a talking point when St Mirren substitute Lewis Guy was taken off in the 80th minute, 18 minutes after coming on. The forward did not look happy as he went straight down the tunnel to be followed by assistant manager Tommy Craig.
Kilmarnock gained revenge over relegated Dundee for denying them a top-six place as they handed Dundee a 3-2 defeat - just the third defeat for new Dens boss John Brown since taking over.
Dundee were relegated last week and there was fresh pain for Brown's side as Kilmarnock struck three times in Tayside through Rory McKenzie, Chris Johnston and Sammy Clingan to secure vengeance for their wrecked top-six ambitions.
Ryan Conroy had cancelled out McKenzie's fourth-minute opener within a quarter of an hour of that early breakthrough but Killie stretched in front again before Mark Stewart added a late consolation for the hosts eight minutes from time.
- Sports & Recreation
- Clydesdale Bank Premier League
- Aaron Doran
- St Mirren
- Dougie Imrie
- Jonny Hayes
- Scott Vernon