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It ended the Brumbies' 11-game winning run at home as the Highlanders made it five straight victories against the ACT men.
Brumbies hooker Folau Faingaa scored a hat-trick of rolling maul tries but it wasn't enough as they failed to take advantage of a yellow card in the second half.
Highlanders winger Patelesio Tomkinson was extremely lucky to avoid a red card after making no attempt to wrap his arms as his shoulder made contact with Tom Banks' head in a tackle.
Referee and former Super Rugby player Nic Berry deemed the initial contact shoulder to shoulder and only opted for the sinbin in the 45th minute, but the replays didn't look good.
The Highlanders hung tough before Teariki Ben-Nicholas crashed over next to the posts after the siren before Josh Ioane slotted the match-sealing conversion.
The Brumbies were forced to make two late changes with Irae Simone and Darcy Swain ruled out with a virus which saw Caderyn Neville and Lenny Ikitau start.
Lock Nick Frost came onto the bench and 18-year-old former schoolboy sensation Reesjan Pasitoa became one of the youngest players in Brumbies history in the 72nd minute.
It was all the Highlanders early and Ioane slotted a simple penalty to give the visitors a 3-0 lead after five minutes.
But the Brumbies settled and scored on their first attacking opportunity inside the Highlanders 22m as Faingaa crossed for his first in wet conditions.
Consecutive penalties saw the Brumbies earn another five-metre lineout and Faingaa, the franchise's leading try-scorer last season, celebrated his second try on 30 minutes.
But the Highlanders immediately hit back from the kick-off when Noah Lolesio was charged down by Jona Nareki who regathered and scored.
Ioane slotted another penalty and the Highlanders took a 13-12 lead into the break before picking up where they left off with another three-pointer in the 42nd minute.
The Brumbies were kept scoreless with their man advantage as rookie five-eighth Lolesio endured a forgettable evening.
Hat-trick hero Faingaa scored his third and a Ryan Lonergan-penalty made it 22-16 in the 74th minute.
The Brumbies had the ball with 15 seconds remaining but the Highlanders won a ruck penalty before breaking the hearts of most of the 7270 fans.