Clint Gutherson starred with a hand in four of the Eels' tries, with the Manly junior sticking the knife into his old club and pushing Parramatta towards the top-four race.
Jake Arthur also set up two second-half tries, turning the match with two crucial second-half plays just a fortnight after being booed by Parramatta fans at CommBank Stadium.
The halfback's effort came after a difficult opening half in defence as Manly cut the Eels' left-edge to shreds and Jason Saab broke the line four times.
The big margin came despite Manly leading 20-14 with 25 minutes to play, before Arthur stepped up and Parramatta ran in the last four tries.
With four rounds to play after this weekend, the Sea Eagles sit four points behind eighth-placed South Sydney and with a far inferior for-and-against record.
"We have to win four-from-four from here," coach Hasler said.
"That would give us a chance, but anything less is not going to work.
"We've got the players to do it. We just have to find a way and just have to win.
"We were certainly in a position to win tonight ... and we didn't. We can't afford to do that."
Making matters worse for Manly is a hamstring injury for Kieran Foran, likely to rule him out of the clash with Gold Coast on Sunday week.
Parramatta, meanwhile, are level on wins with fourth-placed Cronulla and eyeing a second chance in the finals if they keep their winning ways.
The Eels' starting forwards, Junior Paulo and Reagan Campbell-Gillard, were again dominant, while Shaun Lane threw offloads in the lead-up to two tries.
The match wasn't without controversy, with the Sea Eagles being denied a penalty try early in the second half that would have put them 12 points up.
Chasing a loose ball to score, Morgan Harper was ruled to have shielded Will Penisini off the ball before claiming he had been held back on the way to the line.
But still, Manly only had themselves to blame after their late capitulation.
Parramatta started the better through two early tries by Maika Sivo, the first from a Gutherson cut-out ball and the next a grubberkick from the fullback.
Then, after two weeks of drama, the Sea Eagles leapt back to life.
All three of their tries came through last week's boycotting players, with Tolu Koula, Christian Tuipulotu and Saab crossing. Saab also broke the line four times.
And at 20-14 ahead, Manly's season appeared to be reignited.
But two weeks after copping his own jeers from the Parramatta faithful, it was Arthur who stood up for the Eels while filling in for the injured Mitch Moses at No.7.
He first laid on a sweet looping ball for Waqa Blake to pull off a superb flying finish.
And after Gutherson put the Eels ahead, it was Arthur who put the game beyond doubt with a grubberkick for Penisni with 11 minutes to play.
"He's just a young bloke learning his trade. He's fortunate he is in a very good team," coach Brad Arthur said.
"He is behind two very good halves, so he understands his role in the team and he did his job tonight."
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