Having slumped to a 4-1 loss in Tallinn last month, this match was as much about revenge as keeping alive their mathematical hopes of second place in Group C.
In the end under-pressure boss Nigel Worthington saw his side leave Windsor Park with nothing as Konstantin Vassiljev's double, a penalty and a controversial winner six minutes from time, turned the game around after captain Steven Davis' first-half opener.
A chorus of boos rang around the ground at the final whistle, with 'Worthington out' chants mixed with some choice words for the referee, who had allowed Vassiljev's second despite a linesman's flag.
Northern Ireland had a nervy moment in the third minute when Chris Baird failed to contain Tarmo Kink, who surged forward before hooking the ball wide to Dmitri Kruglov.
His awkward cross caused was cleared at the second attempt but it was not a convincing start.
Kink almost put the visitors ahead inside 10 minutes, firing left-footed and drawing a sprawling save from Lee Camp, who had a night to forget when the side's met in September.
Grant McCann returned fire when his 25-yard strike forced a corner in the 15th minute, while Davis was an increasingly lively presence in the centre, winning possession well and supporting Rangers team-mate Kyle Lafferty from midfield.
It was the Ibrox pair who combined to put the hosts ahead, Lafferty breaking down the right and drilling a low cross across the six-yard box. Goalkeeper Sergei Pareiko spilled it and Davis beat two defenders to the ball to bundle home.
Raio Piiroja reminded them of the Estonian threat soon after, producing a neat turn in the area before shooting over.
Worthington was forced to alter his midfield after just half an hour, with Sammy Clingan taken off holding his back and Corry Evans summoned from the bench.
Gareth McAuley was given enough space to charge 60 yards upfield in the 37th minute and, with defenders standing off him as he approached the penalty box, he went for glory only to see his shot charged down.
Estonia started the second half much stronger but wasted two fine chances in the space of the three minutes after the break.
First Kink hit a tame shot following from 10 yards after good work by Ragnar Klavan and then, in the 50th minute, Sergei Zenjov produced an even worse attempt to drag wide with only Camp to beat.
Lafferty was leading the line impressively but a soft yellow card, for use of the elbow, ruled him out of Tuesday's visit to Italy.
With an hour gone, Northern Ireland had still not found their first-half energy and looked increasingly vulnerable on the break.
As a result Chris Brunt and McCourt, who had started as supporting attackers on either side of Lafferty, dropped further and further down the pitch to make a 4-5-1 formation.
Brunt did venture back into the final third in the 65th minute, crossing for Evans, who could not control his header.
Worthington replaced the tiring Lafferty with Warren Feeney but the momentum was still with Estonia.
Piiroja prodded wide from close range as another opportunity came and went for the visitors and Camp was forced into a reaction save by Zenjov.
With 15 minutes remaining Craig Cathcart was penalised for impeding Vassiljev as he cut into the area. He took the penalty himself and drilled into the centre of goal for the equaliser.
Cathcart had the chance to atone with nine minutes left, Brunt heading McCann's long free-kick to the Blackpool defender six yards out.
He did well to get over the ball but there was no power in his shot and Pareiko saved easily.
Instead, it was Estonia who took the points.
It was a glorious long-range strike from Vassiljev but left the Northern Ireland players furious after the linesman was seen to raise his flag in the build-up only to go unheeded.
If there were genuine qualms over the legitimacy of the winner, there was no doubt that it had been coming.
Worthington must now raise his team for a trip to Pescara against the group winners, where he has one final chance to stake a claim for a new deal.