An evening that began worryingly for the young Manchester United striker when his sloppy mistake allowed Stanislav Lobotka to fire Slovakia into a shock lead ended with the crowd singing his name as he sparked England's revival.
Rashford's first international goal came on his debut in a friendly against Australia last May, but his second was of far greater importance as it put England five points ahead of Slovakia at the top of Group F with two games remaining.
The 19-year-old's corner was turned in by Eric Dier for England's equaliser towards the end of a torrid first half for Gareth Southgate's side. Rashford completed the job when he rifled in a 59th-minute winner.
Once again it was a patchy display by England but victory over Slovenia at Wembley next month will mean they can begin booking hotels in Russia.
"We started poorly and I am happy to get a goal that kickstarted the game for us. We were in control for most of the game then," Dier said.
"We weren't aggressive enough and were two seconds behind them in every pass. The way we turned it around was positive."
The expanse of empty red seats in Wembley's upper tiers spoke volumes for the lowered expectations around the England team these days after a succession of major tournament flops.
Even those eternal optimists amongst the 67,000 present must have feared the worst after a woeful opening by the hosts.
The game was only three minutes old when Rashford, preferred to Raheem Sterling after replacing him during Friday's flattering 4-0 win in Malta, gifted possession to Adam Nemec who played in Lobotka to poke the ball past the advancing Joe Hart.
It was the fastest goal conceded by England in a competitive match since San Marino's goal in 1993.
Wembley was stunned and England were rattled as their 17-match winning sequence in World Cup qualifiers looked in peril.
England's attacks were panicky and sporadic, summed up by Alex Oxlade-Chamberlain's hopeless hoof over the bar which brought howls of derision from the crowd.
Had Slovakia reached halftime ahead it would have become a nervous night for the hosts, but they were level in the 37th minute after finally exerting some sustained pressure.
Rashford's corner was poorly struck but Tottenham Hotspur midfielder Dier showed a striker's instinct to get ahead of his marker and sweep a right-footed shot past Martin Dubravka.
Minutes later Rashford forced a great save from Dubravka with a powerful low shot from distance, although England were fortunate on the stroke of halftime when Vladimir Weiss burst through on goal before tumbling under a desperate tackle from Kyle Walker that went unpunished.
There were scares in the second half for the hosts too with Nemec forcing a fine reflex save from Hart.
But there was more cohesion from the hosts and with Rashford causing havoc they deservedly took the lead.
Skipper Jordan Henderson won the ball in middle of the pitch and played the ball to Rashford and as Slovakia's defence backed off he belted a 25-metre effort past the despairing dive of Dubravka to the relief of the Wembley crowd.
England could not find the third goal that would have killed off the visitors but they did enough to earn three vital points.
(Reporting by Martyn Herman, editing by Pritha Sarkar)
