They dominated much of the early period of the game at Forsyth Barr Stadium before struggling to keep out the surging Australians.
The Brumbies led by two points with four minutes to play before they scored a lineout try through Lachlan Lonergan, and Noah Lolesio put the game out of reach with a tricky conversion.
Sam Gilbert kicked a consolation penalty on the buzzer to at least snaffle a bonus point for the Highlanders.
It was hard to spotlight exactly where the Highlanders let this one slip.
They created some good chances and defended well when it was required as they led 11-7 at halftime.
But they spent too much of the second half on the back foot, and made some poor decisions at times.
In fairness to their opponents, the Brumbies got the job done when needed, and flourished in the second half after a long spell focusing on defence.
It was, to be honest, a rather chaotic and unpredictable first half laced with half-breaks and half-opportunities.
The Brumbies were initially dreadful – as if they were still on the plane – while the Highlanders looked sharp in the early exchanges.
After Gilbert had missed an early penalty then immediately made another when the Highlanders snaffled the turnover off the post, the first try came and it was a lot of fun.
Folau Fakatava set up the attack after breaking free from the clutches of some Brumbies forwards.
All-energy No 8 Nikora Broughton, who had a whale of a half as he began a period standing in for the injured Hugh Renton, hacked ahead a loose ball and showed remarkable pace to beat two of his team-mates for the try.
The Highlanders were playing at pace, inspired by Fakatava and he-is-everywhere fullback Jacob Ratumaitavuki-Kneepkens, and anything seemed possible.
Just a pity they could not find the cutting edge to turn their dominance into points.
It almost seemed unfair when the Brumbies, having finally adjusted to Dunedin time and regrouped through some excellent defensive work, capitalised on a period of pressure to score their own try through Tom Wright.
That gave the visitors a boost and they looked more threatening the rest of the way.
The Highlanders made a couple of duff decisions but defended well, led by captain Billy Harmon’s frantic 17-tackle first-half effort.
A second Gilbert penalty and a couple of Brumbies injuries, most significantly to star centre Len Ikitau, sent the home team to the break feeling confident-ish.
What the Highlanders did not need straight after halftime was to see obscenely fast winger Corey Toole get put into a sliver of space for the first time all game . . . oh.
Toole took the patch of open grass and set fire to it as he raced to an in-and-out try to give the Australians their first lead.
When Lolesio added a penalty to make it a six-point game, and the Highlanders promptly committed a couple of frustrating turnovers, the mood under the roof turned flat.
Enter Harmon, possibly still stinging from being dropped last week after a minor disciplinary issue.
Nothing was on when he got the ball. There were five Brumbies defenders head of him.
What did he do? Ran through them all to score.
The conversion restored the lead for the Highlanders but another Lolesio penalty switched things again, setting the stage for a tense final 10 minutes.
Several of those minutes were wasted by reset scrums – elite rugby still needs to sort that out – before the real crunch stage arrived.
The Brumbies got within 5m of the line. Turnover. Then a lineout. And the dagger try.
The Highlanders are on the road next week to play the Chiefs in Hamilton.
The scores
Brumbies 27
Tom Wright, Corey Toole, Lachlan Lonergan tries; Noah Lolesio 3 con, 2 pen
Highlanders 21
Nikora Broughton, Billy Harmon tries; Sam Gilbert con, 3 pen
Halftime: Highlanders 11-7.
