A last-gasp equalizer from Andreas Avraam stunned Portugal and secured a famous draw for the Cypriots in Guimaraes as Portugal assistant manager Agostinho Oliveira took charge for the first time following Carlos Queiroz's suspension.
Cyprus surprisingly went in front after three minutes when Efstathios Aloneftis peeled away from Miguel before audaciously lobbing Eduardo.
Portugal were level five minutes later when Hugo Almeida displayed his aerial prowess by heading a near-post cross from Nani into the far corner of the net.
Cyprus retook the lead on eleven minutes when Raul Meireles got in a tangle, releasing the visitors' record goalscorer Michalis Konstantinou who beat Bruno Alves to the ball to blast home into the net. Suddenly the Portuguese backline that had seemed impregnable in the World Cup was being repeatedly breached.
Raul Meireles then atoned for his previous mistake just before the half-hour with a fizzing strike from 25 yards which deceived Cypriot goalkeeper Antonis Georgallides as it bounced wickedly off the turf.
Portugal completed a superb comeback when Fabio Coentrao crossed from the left and Danny headed home with the help of both Sinisa Dobrasinovic and the crossbar.
But Cyprus was not done yet as substitute and record cap holder Ioannis Okkas made it 3-3 on 57 minutes when he raced onto Charalambides' through ball and coolly slid the ball home past Eduardo with his first touch of the game.
Manuel Fernandes blasted the ball home into the top corner to give Portugal the lead after Ricardo Quaresma's corner was cleared to the edge of the box.
Cyprus snatched a dramatic late equalizer when Eduardo spilled Dobrasinovic's shot into the path of Andreas Avraam who stooped to head the ball home.
Portugal travel to Oslo to face Norway on Tuesday while Cyprus' next qualifier is next month at home to the same opposition.
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