It was the first loss of the season for the defending champion and highlighted a day of upsets in Dunedin premier club rugby when the top three teams were beaten.
Centre Wayne Gibson scored three tries when bottom team Harbour upset third-placed Alhambra-Union 38-25.
A top performance from the pack enabled Green Island to topple second-placed Southern 28-13 and lift the Speight's Challenge Shield.
Fullback Liam Edwards scored 25 points to help Dunedin regain the Larry Salmon Memorial Trophy when Pirates was beaten 55-27.
He leads the premier scoring with 149 points and is followed by Fenemor 125, Cam Rutherford (Kaikorai) 116 and Peter Breen (Alhambra-Union) 104.
University A 31
Taieri 30
No 8 Paul Grant was on fire and played a key role in University A's upset win over Taieri at the University Oval.
The pack displayed discipline and this was epitomised in the last three minutes, when the University forwards drove into the Taieri 22m with a series of pick-and-go movements.
When they were positioned in front of the posts the ball was released to first five Stephen Fenemor, who drop kicked a goal from 30m to win the game.
The students started the game with passion and the first try by centre Fassiu Fuatai came after 90 seconds, after fullback Matt Faddes had counter-attacked up the left flank.
Two minutes later, Grant used his strength to score under the posts and when second five-eighth Harry Corkill scored after charging down a clearing kick, the students led 22-3 after 23 minutes.
A change then came over the game, when No 8 Charlie O'Connell came off the bench and put energy back into the Taieri pack.
The forwards got on top as Taieri clawed its way back into the game and trailed by just six points, 22-16, at the break.
The student forwards regrouped in the second spell, matched Taieri in the tight and at the breakdown, and helped University keep its nose in front.
Prop Tama Tuirirangi had a strong game in the tight and at the breakdown and flanker Dale Jarden was efficient in the tight-loose.
Fenemor kicked two second-half penalty goals to maintain the six-point gap. Taieri took the lead for the first time with just three minutes left, when Ben Nowell kicked a penalty goal.
O'Connell, hooker Will Hurst and centre Michael Collins were the best Taieri players.
University A 31 (Paul Grant, Fassiu Fuatai, Harry Corkill tries; Stephen Fenemor 2 con, 3 pen, drop goal)
Taieri 30 (Matt Davidson, Rhys Collins tries; Andrew Reid con, 5 pen; Ben Nowell pen).
Halftime: 22-16.
Harbour 38
Alhambra-Union 25
Powerful centre Wayne Gibson used his strength to score a hat trick of tries when Harbour beat Alhambra-Union at Watson Park.
The pack dominated the first spell and took two tightheads that were exploited by efficient halfback Johnny Legg, who kept the momentum with Harbour.
A try by hard-working second five-eighth Lex Kaleca just before the break gave Harbour a decisive 21-6 lead at the break.
Alhambra-Union came back strongly early in the second spell and reduced the gap. But this was answered by Harbour with tries after nine and 18 minutes that made the game safe.
Flanker Angus Duckett was efficient at the breakdown and mobile around the paddock and locks Nick Harwood and Sam Ready contributed to Harbour's win.
Lock Matt Kissick led by example and was the best of the Alhambra-Union forwards. First five-eighth Peter Breen kicked four goals but lacked decisiveness in general play.
The Harbour pressure led to too many errors and the Alhambra-Union backs dropped too many passes.
Harbour 38 (Wayne Gibson 3, Lex Kaleca, Nick Harwood tries; Ollie Cuthill 2 con, 3 pen), Alhambra-Union 25 (Tili Puloka, Chris Guild, Nick Wright tries; Peter Breen 2 con, 2 pen). Halftime: 21-6.
Dunedin 55
Pirates 27
The powerhouse scrum, which took three tightheads, was the foundation for Dunedin's eight-try win over Pirates at Hancock Park.
A tighthead just before halftime led to a try by first five-eighth Jesse Toto that gave Dunedin an 11-point buffer, 26-15, at the break.
Dynamic flanker Gareth Evans grabbed the ball, dashed into the red zone and Toto was up in support.
It was the strong Dunedin pack that finally put the boot into Pirates when it won a lineout midway through the second spell and drove 26m for a try by flanker Mitchell Zandstra.
That was the final straw that broke Pirates' resistance and the winning margin blew out after that.
Powerful prop Jacob Ellison, a key player in the Dunedin scrum, was also visible around the paddock with his ferocious tackling and work at the breakdown.
Dunedin blasted away at the start and two tries by fleet-footed fullback Liam Edwards gave Dunedin a 12-3 lead after 10 minutes.
Edwards also converted six of the tries and landed as penalty goal to score 25 points.
It was the strong scrum and the pace of the backline efficiently directed by Toto that was the key to Dunedin's win.
Centre Tumua Ioane added penetration in the midfield and loose forwards Zandstra and Evans were strong at the breakdown and with their support play.
The best Pirates players were backs Kieran Fowler, Glenn Dickson and Marshall Suckling, and openside flanker Naoki Kuwata.
Dunedin 55 (Liam Edwards 2, Pera Gibbs, Tumua Ioane, Jesse Toto, Mitchell Zandstra, Will Henry, Sam Anderson-Heather tries; Edwards 6 con, pen), Pirates 27 (Marshall Suckling 2, Poamo Aiiloilo, Paul Miller tries; Glenn Dickson 2 con, pen). Halftime: 26-15.
Kaikorai 41
Zingari-Richmond 24
First five-eighth Matt Te Tana masterminded Kaikorai's win over Zingari-Richmond in the Tom Richmond Memorial match at Bishopscourt.
He scored one try himself and created three others as the Kaikorai backline outmanoeuvred its opposition.
Fullback Tony Ensor injected speed when he entered the line to score two tries. He ran 55m for his second try.
The Kaikorai romp was helped by some weak tackling by the Zingari backs.
The best Kaikorai forwards were lock Andy Brun in the lineout and flanker Adam Hill for his mobility and support play in the loose.
Kaikorai led 24-10 at the break and put the game out of Zingari's reach with tries by winger Bryce Morgan and centre Logan Moore in the first six minutes of the second spell, to stretch the lead to 36-10.
The best players for Zingari were hard-working flanker Chris Bell, lock Tom Rowe and centre Ben Kent for his defensive work.
Zingari was let down by its lack of discipline in the second spell and an epidemic of dropped passes.
Kaikorai 41 (Tony Ensor 2, Bryce Morgan, Logan Moore, Matt Te Tana, Blair Laughton, Mitch Clarke tries; Te Tana 3 con)
Zingari-Richmond 24 (Tom Rowe, Shota Horie, Daniel Ramsay tries; Mark Hunter 3 con, pen). Halftime: 24-10.
Green Island 28
Southern 13
A performance straight off the top shelf from the Green Island forward pack set up a memorable victory in the Speight's Challenge Shield match at Bathgate Park.
In a Green Island pack that dominated, No. 8 Junior Sala can take credit for being the catalyst for the success through his inspirational work, both in set piece and broken play.
Sala scored the opening try after the ball was kept in hand as it went deep into the Southern half. He was involved again a few minutes later when the same tactic brought a try to prop Andre Clarke.
But after Southern regrouped and came back into the game either side of the break, it was Sala whose barging and deceptive runs from broken play and off the back of the scrum that proved the game-breaker as Green Island scored through Mika Mafi and Sofele Tuiganala.
Sala was well supported by fellow loose forwards Tala Moli and Mafi, while lock Jackson Hemopo was Meads-like in his presence at the lineout and in broken play.
Despite Green Island threatening to run rampant at times, it was a brave effort by Southern, with no shortage of inspiration from captain TJ Ioane. Hooker Johnny Mason and halfback Robbie Smith proved a handful for Green Island defenders.
Green Island 28 (Junior Sala, Andre Clarke, Mika Mafi, Sofele Tuiganala tries; Joe Bartlett con, 2 pen)
Southern 13 (Warren Moffat try; Ben Patston con, 2 pen).
Halftime: Green Island 13-10.