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Campbell-Kirk Waugh decided Regan Coldicott took too long at a throw in and reduced Otago to 10 men, inspiring an Auckland resurgence that eventually clinched a 3-1 result.
Prior to Coldicott's sending off, Otago had led 1-0 since Aaron Burgess scored in the 62nd minute.
The ASB Premiership at the FB Stadium was always going to be an uphill struggle against a star-studded Auckland side which in a month will be playing against the likes of Manchester United in FIFA's World Club Cup championship in Japan.
But Otago showed old-fashioned resilience in a tight defensive shape that Auckland struggled to breach.
Centreback Matt Joy led Otago's uncompromising backline with a superb personal display, closely followed by faultless performances from keeper Liam Little, Craig Ferguson, Thomas Connor and Tristan Prattley.
Sometimes it was a desperate tackle that thwarted Auckland, but as often as not, the Otago defence played calm football and worked the ball forward with good passing movements.
Predictably, Auckland held the lion's share of ball possession, and flattered to deceive with intricate patterns that foundered on Otago's rock-like defence.
Coach Richard Murray was off the bench dancing when his strategy of deep defence and spring-like counterattack punished Auckland by scoring in a classic counterpunching attack in the 62nd minute.
Andrew Ridden set Regan Coldicott free on the left, his pace caused panic, and a driven cross at Auckland's near post had keeper Tamati Williams sprawling, as Aaron Burgess clipped in a well taken goal.
Burgess had been ably assisted by continual lung-bursting runs from youngster Joel Stevens, who several times embarrassed the languid northerners' defensive line led by former international Ivan Vicelich.
Morgan Day also put himself about and showed tight control, fullback Connor slammed on some tackles that caused sparks, and when Victor da Costa went lame, Seamus Ryder enthusiastically joined the fray.
Losing the French midfielder was a disappointment, but nothing like the agony when referee Waugh reduced Otago to 10 men in the 79th minute by sending off Coldicott for a supposed time-wasting "infringement".
Coach Murray could barely control his disbelief.
"We were still one goal ahead, but to lose a pair of legs at that stage was critical. Our whole team had run its socks off, and predictably Auckland started to buzz," he said.
In the last eight minutes, Auckland's jack-in-the box striker Luiz Corrales at last found some daylight and scored twice.
Alex Feneridis also got on the scoresheet.
Auckland coach Ramon Tribulietx praised Otago's tight defensive pattern and the team's spirit.
"We had to just persist with our passing game, and eventually finish better in front of goal which we did," he said.
A shell-shocked Murray praised his troops who definitely "deserved something from the game, through brave defending and scoring a top goal against the league leader, but football can be very cruel, especially with eight minutes to go ..." he said.
Otago United 1
Regan Coldicott 62
Auckland City 3
Luis Corrales 85, 90+2, Alex Feneridis 89