A fiery and entertaining first meeting appeared set for a goalless stalemate at a buzzing Sky Stadium on Saturday.
The crowd of 26,252 was a record regular-season turnout for the Phoenix.
But when Josh Oluwayemi hit an attempted pass straight into Brimmer in the 89th minute, the former Melbourne Victory star and 2021-22 Johnny Warren Medallist pounced.
Brimmer, 26, took a touch then chipped the ball over the Wellington goalkeeper, much to the delight of the travelling Auckland fans.
DRAMA IN WELLINGTON! 🤯— Isuzu UTE A-League (@aleaguemen) Wow. @fc_auckland lead late in the New Zealand Derby 🔥Jake Brimmer pounces on a mistake from Wellington Phoenix 'keeper Josh Oluwayemi to potentially win it for the Black Knights. Watch #WELvAKL live NOW on Paramount+ pic.twitter.com/llSkZvwGvsNovember 2, 2024
Seven minutes later, Luis Twomey beat Hideki Ishige down the left then squared it across goal for Brimmer to slide in and score, maintaining Auckland's perfect start to the season (3-0-0).
Both teams spurned decent chances, with Wellington in particular ruing Ishige missing from point-blank range in the 59th minute.
Phoenix skipper Alex Rufer passed a late fitness test and started in midfield.
The game was a classic derby, with tackles flying in from the opening whistle.
Auckland failed to make the most of their initial dominance, led by captain Hiroki Sakai, before the Phoenix worked their way into the game.
Phoenix star Kosta Barbarouses shot straight at former teammate Alex Paulsen in the 11th minute.
Auckland went close to opening the scoring when Liam Gillion forced a big save from Oluwayemi in the 35th minute.
Auckland striker Guillermo May and Wellington defender Scott Wootton both required treatment, with May bleeding from his eyebrow after a nasty head clash early in the second half.
Both players were able to continue.
Wellington somehow failed to take the lead just before the hour mark when Rufer won the ball, burst forward and lifted a cross to the back post, where Ishige leapt for the ball but bounced his diving header off target.
Wellington continued to press, with Barbarouses and Rufer having late shots blocked by a Dan Hall-led Auckland defence.
Phoenix coach Giancarlo Italiano turned to recruit Marco Rojas late, for his first appearance in 5006 days for the club where he started his career. However, Rojas couldn't find a late winner.
Then, disaster struck for Wellington, with Brimmer, who entered the fray in the 71st minute, scoring twice.
Auckland next have the bye, while Wellington will face Central Coast away next Sunday.
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