After leading by 17 points at three-quarter time, the Bulldogs were overrun by the Saints who kicked three unanswered goals in the last quarter to run out 7.7 (49) to 6.10 (46) winners in front of 43,072 fans.
The win leaves the Saints at a win-loss ratio of 5-1, while the Bulldogs are back in the pack with three wins from six games.
The opening term was reminiscent of the 2009 preliminary final between the two sides, with both teams applying relentless pressure around the ground and showing their desperation at the contest.
After a first-half dogfight, the Bulldogs looked to have the game in their control with their patience going forward and better decision-making around the ground.
But final-quarter goals to Stephen Milne, David Armitage and Sam Fisher gave St Kilda the lead by three points with three minutes to play, and they held on to record a memorable win.
St Kilda coach Ross Lyon praised his side’s character and determination to turn it around after managing only four goals until three-quarter time.
“We couldn’t get any (forward 50) entries in the first half because the pressure was very good and forced us into a lot of handball; (it was an) incredibly high tempo game,” he said.
“We wanted to go quick to avoid a bit of the press and we became a bit reckless and a bit chaotic and non-systematic.”
“To come off two six-day breaks and to play three games in 12 days - the mental toughness of the group is pretty good.”
A stunned Western Bulldogs coach Rodney Eade was left to rue a missed to get four points over a key flag rival, but he took some positives from the demoralising loss.
“Four points are just like gold, because the competition is that even. To be 4-2 would have been great for us. Now we are 3-3 and it just puts pressure on us every week,” he said.
“We have got to win, and we know that. That’s OK, as long as we can bring that effort (we saw tonight).”
“Probably the first three or four weeks we were disappointed we weren’t consistent with our effort. We had that in spades tonight and that is the benchmark of what we have to do every week.”
Lenny Hayes led from the front in the absence of injured captain Nick Riewoldt, amassing 35 possessions.
Hayes was supported brilliantly by Leigh Montagna, who finished with 34 disposals and Nick Dal Santo, who had nine vital final-quarter possessions and helped set up the win.
Sam Fisher - who surprisingly was given the job on Bulldogs forward Barry Hall - was instrumental in the victory, keeping Hall to just one goal while picking up 24 possessions.
For the Bulldogs, it was Jarrod Harbrow who showed experience beyond his years in his best game yet for the red, white and blue, gathering 36 possessions.
It was the 21-year old's coolness under pressure and his dashing run from half back that enabled the Bulldogs to penetrate St Kilda's zone defense on so many occasions.
Despite having St Kilda tagger Clint Jones following him, Bulldogs midfielder Adam Cooney took the points over his opponent, finishing with 36 possessions.
Western Bulldogs 2.2 3.7 6.8 6.10 (46)
St Kilda 1.2 2.3 4.3 7.7 (49)
GOALS
Western Bulldogs: Giansiracusa, Griffen, Hahn, Hall, Higgins, Roughead
St Kilda: Armitage 2, Milne 2, Fisher, Koschitzke, Steven
BEST
Western Bulldogs: Giansiracusa, Harbrow, Gilbee, Cooney, Hahn, Lake, Griffen
St Kilda: Hayes, Goddard, Montagna, Gwilt, Fisher, Dal Santo, Geary
Injuries
Western Bulldogs: Nil
St Kilda: Nil
Reports: Nil
Umpires: Rosebury, Meredith, Pannell
Crowd: 43,702 at Etihad Stadium
The views in this story are those of the author and not necessarily those of the clubs or the AFL.