Ukraine had displaced the Three Lions in first place of Pool H courtesy of their 1-0 triumph over Poland earlier tonight, but England are now just one win away from Brazil 2014 thanks to success at Wembley.
Dejan Damjanovic had brought Montenegro back into the game at 2-1, after Wayne Rooney and an own goal gave the hosts a two-goal cushion, which Townsend restored in the latter stages before Daniel Sturridge completed the scoring from the penalty spot.
Rooney came the closest to breaking the deadlock before the interval, but he could not squeeze the ball in at the near post from six yards after Townsend's powerful drive was parried.
The Manchester United forward did get himself on the scoresheet minutes after the break when he bundled in another rebound, after good work from Townsend and Danny Welbeck, who was also involved in England's second.
He chased after a clever flick on from Sturridge before squaring back towards his teammate, only for Branko Boskovic to intercept by diverting the ball past Poleksic and into the bottom corner.
Montenegro almost pulled one back immediately when Manchester City striker Stefan Jovetic struck the crossbar from 30 yards, and the visitors did reduce the deficit shortly afterwards.
Damjanovic showed good predatory instincts to poke out a foot to guide a mis-hit shot beyond Joe Hart, but any England nerves were ended when Townsend capped his man-of-the-match display with a goal.
The Tottenham Hotspur winger cut inside from the right before dribbling past two Montenegro defenders and shooting in off the post, and there was still time to Sturridge to increase the margin of victory.
The in-form Liverpool forward won the spot kick himself after showing some clever footwork on the byline, and then stepped up to send Poleksic the wrong way from 12 yards.
England now need to better the result of Ukraine, who play San Marino on Tuesday, when they host Poland at Wembley, on the same night, to guarantee World Cup qualification.