England seemed to be heading for victory when midfielder Eric Dier fired in a 20 metre free kick past Russia's veteran goalkeeper Igor Akinfeev yesterday.
But three minutes from the final whistle in the Group B match, Joe Hart and his defence took their eye off the ball. Berezutski rose to meet a cross and sent a looping header into the net.
England players walked off disconsolate while there was more violence in the Stade Velodrome as fans left, adding to the 31 injured in street battles in the Marseille port district earlier.
"It's very disappointing," said Dier. "We gave away a draw. We just didnt see it out the right way. We have to pick ourselves up and go again."
England manager Roy Hodgson handed five Tottenham players their major finals debut for the match, leaving Leicester City striker Jamie Vardy on the bench. England had to battle with the injury-depleted Russians to get ahead in the 77th minute, however.
England won a free kick on the edge of the area when Russian left-back Georgi Shchennikov impeded Spurs midfielder Dele Alli. After Harry Kane's dummy run, Gary Cahill created a hole in the defensive wall and Dier stepped up to fire into the top corner of the net.
It was England's first free kick goal in a major tournament since David Beckham scored against Ecuador in 2006. Hodgson must now be concerned about England's wastefulness however.
The Young Lions' zest, energy and superior footwork helped created a succession of opportunities in a one-sided opening half that had the Russians struggling to keep pace. Adam Lallana wasted their best chance when he drilled wide of Akinfeev's far post just before the half hour.
It looked promising for England when Lallana pounced on Kane's flicked header to send Sterling through the middle, but Igor Smolnikov slid in to clear the danger.
Russia, looking slow in comparison, were bamboozled by Alli's footwork deep on the right.
He set up Rooney, who flicked the ball up to fire a volley that Akinfeev punched to safety eight minutes before the interval.
It brought raucous applause from England's support but, immediately afterwards, even louder calls for the ball to hit the back of the net.
Russia resumed in more positive fashion after the interval and when Aleksandr Kokorin broke free on the right to set up Artem Dzyuba, it took Raheem Sterling to rush in and clear the danger.
England's first-half efforts appeared to have taken a toll, Russia steadily gaining some momentum. An awkward defensive header from Dier at a Russian corner forced Joe Hart into his best save of the match.
Just after the hour Fedor Smolov forced the goalkeeper into action with an ambitious 20-yard drive that crept dangerously wide.
Rooney, however, had fans up out their seats on 71 minutes when he pounced on a poor clearance from a Walker cross to force Akinfeev into a great save that came off the crossbar.
Lallana pounced on the follow-up to fire across the bows, but he was already offside.
England's best chance looked most likely to come from a dead ball situation and when Alli tumbled over Shchennikov, it gave them a golden opportunity.
But Russia refused to throw in the towel and when they broke clear on the left, Berezutski did well to rise above Danny Rose to leave Hart, and England stunned.