Before the last round of games, Russia trailed England by two points with the first two teams going through to the final stages of the tournament. Croatia, in first place, had already qualified.
An English victory or draw against Croatia would have seen Russia miss out on their second major tournament in a row after failing to qualify for the 2006 World Cup. The failure would have hit even harder this time following massive investment in the national game by a range of oligarchs and energy giants.
However, an amazing display of attacking football by Croatia against England at Wembley saw the Balkan side earn a historic 3-2 victory, enabling Russia to leapfrog Steve McClaren's men in the hunt for a Euro 2008 spot.
Russia ground out a 1-0 victory in Andorra, a Dmitry Sychev goal in the 39th minute proving enough for all three points.
The real drama took place at Wembley though, where a catastrophic error by Scott Carson, playing in his first real competitive match for England, gave Croatia a shock 8th minute lead, as the Aston Villa keeper let a Nico Kranjcar shot skim past him on the wet Wembley turf.
Worse was to come though for England, with former CSKA Moscow forward Ivica Olic rounding a stranded Carson to make it 2-0 in the 14th minute. Wembley was in shock. England manager Steve McClaren took shelter beneath his big FA umbrella, but there was no escaping the boos that accompanied the side off the pitch for the half-time break.
The second-half saw the appearance of England icon David Beckham and Tottenham Hotspur's Darren Bent, and the move looked to have paid off when England were awarded a 56th minute penalty, Frank Lampard sending Croatia's other Russian representative, Pletikosa of Spartak Moscow, the wrong way to make the score 2-1.
The fairytale comeback looked to be complete when Peter Crouch hammered home a David Beckham cross in the 65th minute, but Croatia were unwilling to let victory slip away, and a 77th minute shot from substitute Petric restored their 3-2 lead.
Meanwhile, in Andorra, Russia's Dutch trainer Guus Hiddink was watching his side make hard work of minnows Andorra. Leading 1-0 at the break, Kolodin having missed an opportunity to double their advantage with almost the last kick of the half, the side lost captain Andrey Arshavin in the 84th minute, the Zenit star shown a red card for violent conduct.
However, Russia never looked likely of losing their lead, and when cheers from the Russian fans in the stadium signaled Croatia's victory at Wembley, the side calmly played out the last few minutes to complete a remarkable night for Russian football.
Russia seemed to have lost all hope of qualification following Saturday's unexpected 2-1 defeat in Israel, yet Croatia came to their rescue, leading Guus Hiddink to comment that "I feel like we've been playing Russian roulette," at the post-match press conference.
"A miracle has occurred!" said Dmitry Sychev. "That's Russia. We don't do it any other way - it's either everything or nothing!"
In England, Steve McClaren's reign as England boss looked to be at an end as the English FA met at Soho House to discuss his future. An announcement was expected on Thursday morning. McClaren becomes the first England coach to fail to take England to a major championship since 1994.
Slaven Bilic, Croatia's trainer, dismissed talk that England had erred tactically, however, saying to English journalists, "Wake up. You didn't lose the game because of the tactics. I admire your side but we're simply a better team."
Before the game, Leonid Fedun, a LUKoil vice-president and owner of Spartak Moscow, had promised to buy Mercedes for the best Croatian players in the event of the Balkan side's victory in London. However, Ivica Olic rejected suggestions that this, and any other undisclosed financial incentives offered by Russian businessmen, may have contributed to the team's performance.
"The money wasn't important," he said. "We played for our homeland, for Croatia. I have many friends in Russia from my days at CSKA, and my heart beats for the Russians. I'm glad I could give them this present."
"Croatia take Russia with them!" said one Russian sports website, as the largest country on Earth celebrated its most unlikely comeback.
The draw for Euro 2008, to be held in Austria and Switzerland next summer, takes place on December 2.
The 16 teams who have qualified are -