WIGAN allowed the chance to climb top of the ladder slip through their fingers in agonising fashion.
They led 14-12 when Josh Jones broke their hearts with less than three minutes remaining.
It was a knockout blow at the end of an enthralling, nerve-shredding clash between these Super League heavyweights.
Level 6-6 at the break, Wigan nosed in front with a penalty before George Williams powered them further ahead with a scintillating try.
But Adam Swift countered to cut the visitors’ lead to 14-12 and set up a dramatic finish.
Jones settled the contest when he leapt above Matty Bowen to a high ball and dashed over.
Manchester United icon Ryan Giggs - a Wigan fan - watched on as Shaun Wane’s players fell to a second-successive derby defeat.
And it leaves their hopes of finishing top of the ladder once again hanging in the balance.
Given Leeds’ superior for-and-against, the Warriors must now beat Castleford next week - and hope the Rhinos lose to Huddersfield - if they are to get their hands on the league leaders’ shield.
But this contest could easily have gone their way, and the disappointing result came at the end of a pulsating contest.
There were plenty of dropped ball from both sides, but they only served to heighten the drama, not diminish it.
On a night when union’s World Cup launched at Twickenham, league bosses must have been delighted with the treat these two rivals served up for the Sky Sports cameras.
As predicted, Wane brought Sean O’Loughlin and Bowen back into the team, while St Helens recalled Mose Masoe in place of injured Alex Walmsley.
Saints hadn’t won at home since July, and Wigan hadn’t won a non-Easter game at St Helens since 2003 - something had to give.
And from the opening set it was evident both outfits would not lack passion.
On a mild evening, in front of an electric crowd, they went toe-to-toe, slugging it out with as much energy and power as two seasoned heavyweights.
Both sides had put a strong emphasis on defence in the build-up, and it showed - the scoreline was just 6-6 at the break.
Bowen pounced on Joe Greeenwood’s spill for the game’s first clear chance, before Jordan Turner had claims for a try waved away by the video referee.
Joel Tomkins broke the deadlock in the 13th minute, charging onto Matty Smith’s sharp pass, and wrong-footing Adam Quinlan, to pace over for a try, converted by Bowen.
The visitors pushed for a second, forcing three successive drop-outs, but Saints did well to absorb so much pressure on their line.
In the 34th minute Luke Walsh drew level when he squeezed beyond Lee Mossop, and darted through for a try he converted.
In a dramatic finish to the half, two skirmishes - both involving Tony Clubb - erupted, to set the tone for a ferociously-fought start to the second half.
But it was a touch of fortune which allowed them to poke in front, referee Robert Hicks awarding Wigan a penalty for obstruction - when Mossop appeared to knock-on - and Bowen slotted the ball between the uprights.
If there was a touch of luck to that score, the next was all down to the magical footwork of Williams, who weaved through the defence, scorched down field and wrong-footed Quinlan - giving a quick salute to the travelling faithful - before sliding over. Bowen’s conversion made it 14-6 with less than half-an-hour remaining.
But moments later the Wigan No.1 had the ball stripped in a tackle, gifting Saints unexpected possession, and their offloads stretched the visitors’ line and Swift stepped through the covering defence.
Walsh converted from the sidelines to cut the Warriors’ lead to a slender two points.
O’Loughlin won a penalty in Saints’ territory, but the line didn’t creak under a heavy bombardment as the game hurtled into the final 10 minutes.
The thrills kept coming, fast and furious, as Quinlan’s break was hauled back for a harshly-ruled forward pass and then Gildart was held up over the line - only for Jones to have the final say.
Wigan finish the regular season next Friday, at home to Castleford.
St Helens: Quinlan; Makinson, Percival, Jones, Swift; Turner, Walsh; Amor, Roby, Savelio, McCarthy-Scarsbrook, Greenwood. Subs: Masoe, Vea, Flanagan, Richards.
Wigan: Bowen; Charnley, Bateman, Gildart, Burgess; Williams, Smith; Crosby, McIlorum, Flower, Tomkins, Patrick, O’Loughlin. Subs: Gelling, Powell, Clubb, Mossop.
Referee: Robert Hicks
Starman: George Williams