Lyon masterminded a 61-point win over Fremantle eight weeks ago in Melbourne, and another upset was brewing on Sunday at Optus Stadium as the Saints opened up a 14-point lead early in the final quarter.
St Kilda dominated the clearances 39-16 across the opening three terms, but Fremantle won the key stat 15-7 in the final quarter to make their move.
Sean Darcy marked a low ball and kicked truly to start the onslaught.
Luke Jackson, Josh Treacy and Isaiah Dudley followed it up with their own set shots as Fremantle shot out to a 10-point lead.
The margin was pegged back to just six points with 49 seconds remaining when Mitch Owens snapped truly, but Fremantle won the next centre clearance and Jackson pulled off a stunning mark in attack to ice the 11.15 (81) to 9.15 (69) win in front of 41,600 fans.
Fremantle's sixth straight victory improved their record to 10-5 ahead of a challenging away clash with Sydney.
St Kilda (5-10) fell further adrift of the top eight, in 15th spot.
Saints ruckman Rowan Marshall was superb, winning 10 clearances to go with 21 disposals and a goal.
Treacy kicked three goals for Fremantle, and Jackson chipped in with two in the last quarter. Jordan Clark had a game-high 31 possessions, and a goal.
Much pre-match talk centred on whether Ross Lyon would send tagger Marcus Windhager to Caleb Serong or Andrew Brayshaw.
The answer was neither, with Windhager released of his tagging duties, and the likes of Jack Macrae and Hugo Garcia instead left to mind their more highly-vaunted opponents.
Brayshaw tallied 25 possessions and just two clearances, while Serong was restricted to 18 disposals but lifted in the final quarter to finish with nine clearances.
Serong and Brayshaw combined for just seven disposals in the first quarter, but two goals to Treacy ensured the Dockers took a three-point lead into the break, with St Kilda's inaccuracy (1.5) proving costly.
Treacy fired up the crowd early in the second term with a team-lifting run-down tackle on St Kilda speedster Nasiah Wanganeed-Milera.
Former Docker Liam Henry was loudly booed each time he touched the ball. He answered back with a 'shoosh' motion to the crowd after thrusting St Kilda into the lead with a second-quarter goal.
The most magical moment of the second quarter belonged to Marshall, who volleyed the ball direct from a ruck contest to kick his first goal of the match.
Fremantle went into the long break with a three-point lead, but the first half had definitely been played on St Kilda's terms.
Shai Bolton's superb set shot from near the boundary line to start the third quarter was quickly nullified as St Kilda kicked the next three goals to take a shock eight-point lead into the final change.
The clearance count read a staggering 39-16 in favour of St Kilda at three-quarter time, but Fremantle turned the tables with a stunning final- blitz that yielded four goals in the space of five playing minutes.
Lyon, the most successful coach in Fremantle's history, was booed by home supporters when shown on the stadium's big screen in the final quarter, in his first match against the Dockers in Perth since being sacked by the club in 2019.
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