In a shootout that featured eight lead changes, the Demons overturned a 15-point deficit during the final term to win a late home-and-away season classic 17.11 (113) to 17.7 (109).
The Dockers led for 70 minutes during their final game at the MCG before a possible grand final in September, but Melbourne captured all the momentum late as Fremantle suffered just their third defeat of the season.
Harrison Petty turned from villain to hero for the Demons with two crucial last-quarter goals after giving away a 50m penalty and missing a gettable shot.
Wingman Harry Sharp also played a massive role in Melbourne's final-quarter surge, finishing with three goals.
"Wharfie time" at Optus Stadium has captured the imagination of the AFL world during Fremantle's rise to the top this year.
But Melbourne coach Steven King believes his club's supporters are also creating a hostile atmosphere for the opposition, with the Demons record at the MCG this season 10-1.
"Demon time at the end of the game there, (it) was heaving," King said.
"We've played pretty well here all year, and I've got no doubt it's that members' wing (when) that starts rocking, the boys feed off that energy.
"It's (Demon time) is probably me trying to play up that we've got something special as well.
"It's obviously a privilege to play at the MCG every week, and we want it to be a bit of a fortress for us."
The match was a thrilling battle of capitalising on centre square dominance, with Melbourne captain Max Gawn going up against Fremantle superstar Luke Jackson in a blockbuster duel.
Both sides traded blows out of the middle all day, but the Demons kept going for longer.
Gawn, Kysaiah Pickett and Tom Sparrow all performed brilliantly for Melbourne, who will avoid dropping into the wildcard zone this weekend.
If the Demons can win their remaining games against Port Adelaide and the Western Bulldogs they will be assured of a week off before finals.
Despite the loss, Fremantle's triple-threat forward line emphatically answered questions about whether they could do it on the MCG.
Jye Amiss (five), Patrick Voss (four) and Josh Treacy (two) combined for 11 goals and looked threatening throughout.
Amiss and Treacy both ticked past 50 goals this season, making them the first Fremantle pair to achieve the feat together since Matthew Pavlich and Jeff Farmer in 2006.
Voss is putting together a fearsome record at the MCG, kicking 15 goals across only three career games at the venue.
The Dockers will still almost certainly claim the minor premiership, ahead of games to round out the home-and-away season against Adelaide and Carlton.
Captain Alex Pearce (managed) will likely return to face the Crows after being sorely missed in the Dockers' defence.
"Clearly he would have helped," Fremantle coach Justin Longmuir said of Pearce.
"Saves us a goal, which probably wins us a game.
"Probably lacked a bit of leadership down there and we weren't able to turn the tide.Â
"We were average behind the ball, our back six.
"For Petty to take that mark into the goal square in a pack, pretty much uncontested late in the game, we've got to get body on him in that moment and and get that through."
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