The Arsenal defender bundled home skipper Thierry Henry's cross 13 minutes into extra-time, although the Barcelona star appeared to handle before he picked out his team-mate in the middle.
It was tough on Ireland who had levelled the aggregate scores through Robbie Keane's 32nd-minute strike and threatened to take the lead as John O'Shea and Damien Duff passed up glorious opportunities.
Slovenia reached the 2010 World Cup finals at the expense of nine-man Russia thanks to Zlatko Dedic's 44th-minute goal.
The Bochum striker toe-ended in Valter Birsa's cross a minute before half-time in what proved to be the game's only goal to spark jubilant scenes at the Gradski Vrt stadium.
Russia, who had Aleksandr Kerzhakov and Yuri Zhirkov sent off in the second half, were left to rue some poor defending and an overall disjointed performance.
The warning signs were there for Hiddink as early as the fourth minute, when a simple through-ball from Birsa inexplicably cut open the Russian defence and allowed Milivoje Novakovic a clear sight of goal, but his finish lacked confidence and was straight at keeper Igor Akinfeev.
Six minutes later there was a huge let-off for Russia when Andraz Kirm's cross from the left struck the leg of the hapless Sergei Ignashevich, who saw the ball rebound off the post with Akinfeev motionless.
As the clock ticked towards half-time, the home support erupted as Dedic got behind two Russian markers to turn in Birsa's cross and give Slovenia the lead at the break.
Hiddink made two changes at half-time, bringing on Sergei Semak and Aleksandr Kerzhakov for Pavlyuchenko and Yanbaev.
But Russia's night went from bad to worse when the Dinamo Moscow striker was shown a contentious red card by Norwegian referee Terje Hauge on 66 minutes.
Zhirkov's cross from the left was whipped in dangerously towards Kerzhakov, who got the better of his marker and slid in on goalkeeper Samir Handanovic, appearing to make a legitimate stab at the loose ball.
The challenge was interpreted as dangerous play by the referee, and closer inspection of the incident also appears to show Slovenia defender Bostjan Cesar strike Kerzhakov in the face, while goalkeeper Handanovic chipped in with a retaliatory hand aimed at the striker.
Hiddink reacted by throwing on another striker, Pavel Pogrebniak, in place of Diniyar Bilyaletdinov and the Stuttgart man almost made an immediate impact with a 12-yard header from Arshavin's cross that was held by Handanovic.
There were more ugly scenes in stoppage time as Zhirkov was shown a second yellow card following an altercation with a Slovenia substitute on the by-line.
Dimitris Salpigidis scored the only goal as Greece clinched a place at the 2010 World Cup courtesy of a narrow 1-0 victory over Ukraine at the Donbass Arena in Donetsk.
Salpigidis timed his run to perfection just after the half-hour mark to clip a composed finish beyond Ukraine goalkeeper Andrei Piatov, following Celtic striker Giorgos Samaras' superb through-ball.
Alexei Mikhailichenko's side, needing to score twice to keep their qualification hopes alive, penned the Greeks in the own half for long spells in the second half but failed to breach a visiting rearguard inspired by goalkeeper Alexandros Tzorvas, who made a string of fine saves.
It is the first time Greece, the 2004 European Champions, have qualified for a World Cup since 1994 in the United States.
Antar Yahia's spectacular goal earned Algeria the final African qualifying spot in South Africa.
The centre-half volleyed home five minutes before half-time and a solid rearguard effort in the second half kept out Egypt for a 1-0 victory.
Emad Meteab had the best chance for Egypt but was denied by impressive Algeria keeper Fawzi Chaouchi.
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