
Steve McClaren's side went into the match knowing a win would secure a finals berth in Austria and Switzerland next summer and appeared well on track when Wayne Rooney scored after 29 minutes with a fierce volley.
Steven Gerrard should have made it 2-0 early in the second half before Russia were awarded a penalty on 69 minutes after Rooney was harshly adjudged to have fouled Konstanin Zurianov in the area.
Roman Pavluchenko scored from the resultant spot-kick to level the scores and he made it 2-1 to Russia four minutes later, poking the ball home from close range after Paul Robinson could only parry Alexei Berezutsky's shot.
England pushed forward in desperate search of an equalizer but Russia held on for a vital victory.
The result means Russia move onto 21 points, two behind England but with a game in hand and five behind leaders Croatia.
Guus Hiddink's side can guarantee qualification if they manage to beat Israel and Andorra in their final group matches.
Croatia, meanwhile, need only a draw in one of their last two matches against Macedonia and England to qualify while England have to beat Croatia at Wembley in their final game and hope one of their opponents slip up.