A ninth successive home win would have capped a remarkable turnaround for a Wanderers team placed 20th at the start of February, and one point looked like being enough at the Reebok on Saturday until Anthony Knockaert gave Leicester a last-gasp 3-2 win over Nottingham Forest to secure sixth place for the Foxes.
Blackpool attacked with a verve rarely seen since their stint as early season pace-setters and fine goals from Matt Phillips and Ludo Sylvestre had them 2-0 up after 35 minutes.
That lead appeared safe as the interval approached, but Chris Eagles and recalled striker Craig Davies were on hand to haul Wanderers level.
Darren Pratley and Lee Chung-Yong passed up chances to give Bolton the win they ultimately needed - misses they were left to rue after Knockaert's late intervention.
Simon Cox's early goal for play-off rivals Forest meant Bolton had to find their feet.
But Blackpool made the breakthrough in stunning fashion after 21 breathless minutes - Phillips emerging from slick one-touch interplay involving Tom Ince and Gary Taylor-Fletcher to lash left-footed into the top corner.
The visitors went further in front before the break. Paul Ince's side once more benefited from static defending with aplomb - Neal Eardley's lofted cross to the edge of the area was crisply volleyed home as Sylvestre claimed a fourth goal in six matches.
In an attempt to turn things around, Dougie Freedman sent on striker Marvin Sordell in place of Robert Hall eight minutes before the break and his team unleashed a staggering turnaround in injury time.
Two of the outstanding performers in Bolton's late-season rally combined to reduce the arrears as Eagles arched an excellent side-footed finish into the top corner from 18 yards after Marcos Alonso raided down the left.
And in the last act of the half, Davies' hopeful strike from distance took a wicked deflection off Stephen Crainey to leave Gilks with no chance and send the Reebok into raptures.
The momentum kept up after the break. Davies and Eagles tried their luck from distance but an open game equally suited Blackpool, for whom Ince's influence was growing.
Gary MacKenzie was forced into an acrobatic clearance for Blackpool, Matt Gilks did well to push Alonso's 30-yard free-kick clear and Lee was guilty of a glaring miss in the 84th minute.
Hearts were in mouths at the other end when Adam Bogdan tipped over a rasping Sylvestre strike from the corner of the box but worse news arrived from the City Ground.
Wanderers surged forwards once more during five additional minutes but David Wheater could not turn home a cross from fellow sub Tom Eaves, leaving them agonisingly short.