Chasing 259, David Warner played a lone hand with 99 as Australia capitulated from 4-189 in the 36th over to be all out for 254 and down 3-1 in the five-match series.
The margin could also have been far worse, if not for Pat Cummins’ 35 and Matthew Kuhnemann scoring 14 from the final over off Dasun Shanaka before being caught in the ring on the final ball.
But it couldn’t paper over Australia’s uphill battle against spin.
Seven wickets fell to the slower bowlers, as Sri Lanka played five turners and sent down 43 overs from them on a used wicket that spun well into the night.
Just over a week out from the first Test in Galle, the hosts’ win will likely confirm the blueprint on how they plan to beat Australia in the red-ball format.
Legspinner Jeffrey Vandersay took 2-40, offspinner Dhananjaya de Silva 2-39 and mystery spinner Maheesh Theekshana 1-40.
Warner meanwhile had looked in control after Aaron Finch (0) Mitch Marsh (26), Marnus Labuschagne (14) and Alex Carey (19) all came and went.
The opener was cagey in the early overs, before throwing his hands at mystery spinner Theekshana and taking him on.
He hit 12 boundaries in his knock, going hard through the covers and driving superbly.
And when he reached 99 Warner looked almost certain to end the longest century drought of his international career, which now sits at 48 innings across all formats.
But the match then swung violently in Sri Lanka’s favour, handing them their first bilateral one-day series win over Australia at home since 1992.
With Warner at the non-striker’s end Travis Head (27) was bowled by Dhananjaya, before Glenn Maxwell was trapped lbw by Theekshana next over.
And when Warner finally got back on strike, Dhananjaya drew him off balance and beat his outside edge to have him stumped.
Cameron Green followed shortly after, before Cummins (35) and Kuhnemann’s late efforts.
The collapse will no doubt have evoked memories of the 2016 Test tour for the locals, when Australia struggled to combat the spin in the 3-0 series loss.
“This is extreme spin; you don’t usually see these type of wickets,” Warner said.
“You only see them here. India is completely different. They don’t turn like that. They’re actually good wickets. And they turn later on day three or four (of Tests).
“So everyone has to prepare as well as they can. It’s about being busy.
“It’s about committing.
“It’s about batting long periods of time. And unfortunately, in the subcontinent, one little mistake will cost you.”
The good news for Australia on Tuesday was that their two best players from 2016 are returning to fitness, with Mitchell Starc and Steve Smith both sighted in the nets with a red ball after finger and quad injuries.
Cummins also bowled nicely on field, taking 2-37 and unlucky not to have another wicket early when he hit Charith Asalanka’s leg stump with the left-hander on one.
However, the bail did not fall off, allowing Asalanka to lead Sri Lanka from 3-34 to 258 with his maiden international century of 110 from 106 balls.
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