The margin was just five points in favour of Fremantle early in the final quarter after Port forward Katelyn Pope shook off two tacklers to kick truly.
Whether Fremantle could hold on against the breeze was a huge question, but they needn't have worried.
Miller caught Shineah Goody holding the ball close to goal to extend the margin back out to 11, before Gabrielle Biedenweg-Webster tumble-turned her way free of a tackler before popping up to kick another.
Sunday's 7.4 (46) to 3.6 (24) win was sealed when Miller kicked her third goal late in the match, sparking celebrations among the Dockers.
Bowers missed all of last season due to pregnancy, but it was like she never left as she compiled 22 disposals, six clearances and 14 tackles as she celebrated her 50-game milestone in style.
Gabby Newton (22 disposals) was also huge in what was also her 50th game, while captain Angelique Stannett kicked two goals in her return from a knee reconstruction.
Stannett's leadership was on full display in the third quarter when she pulled off three consecutive smothers.
"That is the reason she's the skipper. She's amazing," Bowers told Fox Footy.
"I love these girls, and I loved watching them win last year, but it's definitely nice to be out here with them.
"This group is special, and hopefully I keep winning with them."
Port ruck Matilda Scholz (25 hitouts, seven clearances, 12 disposals) won her tap duel against All-Australian Mim Strom (16 hitouts, two clearances, 17 disposals).
Justine Mules-Robinson kicked two goals for the Power.
Port were dealt a blow late in the first quarter when Amelie Borg suffered a game-ending injury to her left ankle, with the defender seen on crutches a short time later.
Fremantle forward Tunisha Kikoak was concussed in the second quarter after copping a heavy hit in a marking contest.
The Dockers made a flying start to the match courtesy of goals to former skipper Miller and current captain Stannett.
The second quarter lit up when Port's Goody delivered a huge bump on Sarah Verrier.
Verrier popped straight back up to gain her revenge, and a heated wrestle soon followed.
Fremantle opened up a 17-point lead early in the third term when Megan Kauffman snapped truly.
But with Scholz giving Port's midfielders silver-spoon service, the home side closed to within a kick early in the final quarter, before Miller and company brutally slammed the door shut.
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