Cooper will run out onto the same Eden Park pitch where he sustained a serious knee injury in the World Cup's bronze medal decider against Wales, capping a miserable tournament for the mercurial playmaker in his last appearance for the Wallabies.
Overlooked for Australia's June Tests against Scotland and Wales, Cooper returns to a side desperate for some spark after a dismal 27-19 loss to the All Blacks in Sydney last week.
His inclusion adds spice to the match at Eden Park, where the Wallabies have not beaten the hosts since 1986 and where the fly-half was targeted by the All Blacks, and their fans, in the 20-6 semi-final loss at the World Cup.
Greeted by a barrage of jeers from the crowd, Cooper started that match by kicking the ball into touch and played poorly thereafter as the All Blacks shut down his time and space.
He ended it by being unceremoniously dumped over the touchline by winger Richard Kahui as the crowd chanted "four more years", in reference to the taunt by former Australia scrum-half George Gregan during the semi-final defeat of the All Blacks at the 2003 World Cup.
Australia must win Saturday's match to ensure they have any hope of regaining the Bledisloe Cup. The All Blacks have held the trophy symbolising trans-Tasman supremacy since 2003.
The third match in the series will be played in Brisbane on October 20, separate to the Rugby Championship competition with South Africa and Argentina.
Cooper will link with Queensland Reds team-mate Will Genia, who will captain the side after openside flanker David Pocock was ruled out following knee surgery after the Wallabies' 27-19 loss to the All Blacks in Sydney last week.
Berrick Barnes moves back to inside centre to accommodate Cooper, while full-back Kurtley Beale has been dropped from the starting line-up after a poor performance in Sydney.
Adam Ashley-Cooper moves into Beale's place at full-back, allowing Drew Mitchell to come in on the wing.
Coach Robbie Deans has given his forwards a chance to vindicate themselves after they were out-muscled by the All Blacks last week at the Olympic stadium with the only two changes to the pack injury-enforced.
Michael Hooper will replace Pocock on the side of the scrum, while Ben Alexander comes in at tighthead prop for Sekope Kepu, who suffered a knee injury during training this week.Hooker Tatafu Polota-Nau was originally named in the side but withdrawn later after he pulled up following training at Leichhardt Oval in inner-west Sydney. He was replaced by Stephen Moore.
Polota-Nau could still be included in the replacements bench after the Wallabies' final training run in Auckland on Friday.
Deans will name the replacements after that session.
"The team comes first," Polota-Nau said. "If I can get through training tomorrow, I'll be available for the bench, but everyone needed to know what was going on now, the team needed to be certain who was playing hooker, and I couldn't provide that.
"This is a massive game for us. Everyone needs to be at their peak if we are to give ourselves a chance."
Team: 15-Adam Ashley-Cooper, 14-Drew Mitchell, 13-Rob Horne, 12-Berrick Barnes, 11-Digby Ioane, 10-Quade Cooper, 9-Will Genia (captain), 8-Scott Higginbotham, 7-Michael Hooper, 6-Dave Dennis, 5-Nathan Sharpe, 4-Sitaleki Timani, 3-Ben Alexander, 2-Stephen Moore, 1-Benn Robinson
Replacements: To be confirmed.
- All Blacks