WaiBOP, another new entity in this year's competition, led 2-1 at halftime and extended their advantage on the hour through Maksim Manko. But, after Marcel Corbera was sent off for a second bookable offence, Elijiah Neblett headed home Wanderers' second to set the stage for a grandstand finale.
The shadow New Zealand under-17 side piled on the pressure in the last 15 minutes but it was referee Mirko Benischke who played the biggest part in the breakthrough, awarding a questionable penalty after goalkeeper Andrew McNeil punched clear.
McNeil almost went from villain to hero after saving Nick Sugden's spot kick, before the striker tucked home the rebound to set off celebrations from the home side and protestations from the visitors.
The equaliser saw Wanderers pull within a point of WaiBOP but both sides are already some way behind the senior Auckland pair. At Kiwitea St on Saturday, City recovered from dropping their first points of the season last weekend to hand Waitakere a maiden defeat in the new campaign.
The defending champions had conceded just once from three games but it was their attack which was blunted as Auckland continued their recent dominance in the derby.
Waitakere struggled to create clear-cut chances for much of the match and, while Auckland hardly ran rampant, the hosts controlled proceedings after Chris Bale's wonderful opening strike.
Auckland could have increased their lead shortly after halftime when Ryan de Vries earned a questionable penalty against his former side, but Danny Robinson spectacularly tipped Adam Dickinson's low attempt around the post.
The points weren't safe until Darren White's stoppage time strike, allowing Auckland to turn their attentions to their Club World Cup qualifier against host club Raja Casablanca.
Elsewhere, Team Wellington edged Hawkes Bay 2-1 in Napier, while Canterbury's 3-0 defeat condemned Southern United to a fourth straight defeat to begin the season.
Results from round four of the ASB Premiership:
Saturday
At Kiwitea St, Auckland
Auckland City 2 Waitakere United 1
Sunday
At Bluewater Stadium, Napier
Hawkes Bay United 1 Wellington 2
At Rugby Park, Invercargill
Southern United 0 Canterbury United 3
At North Harbour Stadium, Albany
Wanderers SC 3 WaiBOP United 3