Thumped 40-0 by the Roosters just five weeks ago, the Sharks completed a remarkable turnaround at Remondis Stadium - the victory set up by a brilliant opening half when the home side ran away to a 26-0 lead.
Conceding 30 points for the first time this season, the Roosters are now ahead of arch-rivals South Sydney by points-differential alone - setting up a potentially epic final round encounter between the two sides in just under a fortnight.
But this was Cronulla's time to stamp their premiership credentials, as they guaranteed at worst home-ground advantage in week one of the finals.
The tone was set in the opening set when the brilliant Todd Carney landed a 40-20 and then a delicate grubber for Paul Gallen to score in a dream start for the home side.
The half will be remembered for the three tries in the final nine minutes of the stanza that broke open the contest, but it was the desperate goalline defence which preceded the late onslaught which defined Cronulla's mentality.
Having repelled the best attack in the competition time and again, Cronulla took late advantage as the Roosters' discipline unravelled with Sonny Bill Williams giving away four first half penalties.
The giant Kiwi was unlucky to collect the last for a strip however, with replays indicating Ben Pomeroy had knocked on - but it proved crucial as the Sharks went on a points-feeding frenzy.
Michael Gordon, Johnathan Wright and Chris Heighington all crossed for tries against a rattled Roosters outfit - the last try summing up their effort with Heighington performing a one-on-one strip from Shaun Kenny-Dowall from ten metres out before waltzing over the line.
The Roosters threatened with two tries inside the opening 12 minutes of the second period, but their momentum was punctured when Roger Tuivasa-Sheck was denied what would have been a spectacular four-pointer due to a Daniel Tupou obstruction.
Stand-in captain Mitchell Pearce argued his winger had nowhere to go - and no longer did the Roosters as Carney added three penalty goals to take the lead beyond three converted tries before two late tries added some respectability for the visitors.
Sharks coach Shane Flanagan claimed the victory laid to rest any questions as to his side's premiership credentials.
"We proved that tonight but in semi-finals everyone steps it up a gear," Flanagan said.
"We're in there and we'll give it a fair crack.
"You don't get the opportunity to beat the team coming first often."
Said Gallen of his side's ability to overcome a side which had won seven games on the trot:
"We really respect them but we don't fear them and we took that attitude into it.
"I thought we took it to them and maybe got the better of them."
Roosters coach Trent Robinson was clearly irked by the Tuivasa-Sheck no-call.
"We got a DVD at the start of the year that said the guy can't dig a hole (and disappear) ... says so that's a try," Robinson said.
"That's a really poor call from them, they got that wrong.
"We had some momentum, it would have made them a bit nervous.
"We weren't good enough tonight, they were good, but that's not good enough from the refs."
CRONULLA 32 (P Gallen M Gordon C Heighington J Wright tries T Carney 8 goals) bt SYDNEY ROOSTERS 22 (D Tupou 2 M Jennings D Mortimer tries J Maloney 3 goals).
Referees: Henry Perenara, Ashley Klein.
Crowd: 11,418 at Remondis Stadium.