It secures eighth position for the Power on the ladder after it was briefly pushed out by Carlton overnight, while putting paid to an eight-game losing streak at the venue.
But it was an 'Jekyll and Hyde' performance from the Power, which led the Saints by 39 points at the long break before squandering its lead in the second half.
Justin Westhoff, fresh from a one-week suspension received for striking the last time he was at Etihad Stadium, was Port's hero.
He took three critical marks in the final term - two in defence - to stifle St Kilda's late momentum.
Port's 'Doctor Jekyll' football was on full display in the opening two quarters.
Port's 'Doctor Jekyll' football was on full display in the opening two quarters.
It booted two fast goals to open proceedings through tall forward John Butcher.
The Saints responded to level the scores at 14 apiece before the Power clicked up a gear and ran the term out with five consecutive majors.
It was Port's best first-quarter performance since Round 21, 2009 when it kicked ten goals against the Brisbane Lions, and things were looking good for Ken Hinkley's men when they carried a 39-point buffer into the long break.
But just as the Lions did on that fateful Saturday night at the Gabba four years ago, the Saints responded to the Power's lead and slowly chipped away throughout the back end of the match.
The Power's 'Mister Hyde' second half was a stark contrast to its opening quarters.
Indeed, it was as if St Kilda had stolen Port's first-half ability to win the ball and play a competitive brand of pressure footy, such was the turnaround in form between the two sides.
The substitution of Jake Neade from the game in the third quarter injected paceman Kane Mitchell into the match and he provided a small spark to the Power.
His goal was the Power's only major to interrupt the Saints' five for the term.
Things weren't much better for Port in the final quarter as the Saints controlled the play and hit the lead for the first time all match with less than 10 minutes remaining.
Things weren't much better for Port in the final quarter as the Saints controlled the play and hit the lead for the first time all match with less than 10 minutes remaining.
But a handful of heroes rose to the challenge for Port and it was Jasper Pittard who took the game on in a thrilling passage of play to win a free and 50-metre penalty; kicking his first goal and reclaiming the lead for the Power.
It would prove a deciding element of the game, along with the match-defining marks of Justin Westhoff.
The high-flying Westhoff capped off a strong return game with several Leo Barry-like efforts to carry his team to the line and avoid memories of that infamous 2009 capitulation.
The Power returns to Adelaide on Sunday ahead of its Round 18 game against the Brisbane Lions at AAMI Stadium.
FINAL SCORES
Port Adelaide 7.4 10.8 11.10 14.13 (97)
St Kilda 2.2 4.5 9.9 13.14 (92)
Goals: Butcher 3, Wingard, Westhoff 2, Lobbe, Schulz, Monfries, Gray, Mitchell, Pittard
Substitute: Kane Mitchell replaced Jake Neade in the third quarter
