England manager Roy Hodgson pulled a surprise by putting Townsend in the starting lineup for his first cap. Four months ago, Townsend withdrew from the squad for the European Under-21 championship before receiving a one-month ban and a fine of $27,000 for breaching betting rules.
But a strong start to the season with Tottenham saw Townsend force his way into consideration for the team.
From the start Friday, the 22-year-old Townsend used his pace down the right side to trouble the Montenegro defense.
England was facing a goalkeeper who, like Townsend, recently served a ban for breaching rules. Vukasin Poleksic's two-year suspension was for failing to report that match-fixers approached him before a Champions League match.
Townsend ensured England made the perfect start to the second half, charging down the right wing and sending a cross that wasn't cleared. Welbeck's shot was stopped, but Rooney put in the rebound in the 49th minute.
It was the Manchester United striker's sixth goal in five qualifiers.
A backheel from Sturridge in the 62nd minute released Welbeck on the left flank, and his cross was inexplicably sent into the net by Boskovic when under no pressure.
England seemed to be cruising when Montenegro pulled one back. Against the run of play, Damjanovic turned Fatos Beqiraj's shot beyond keeper Joe Hart in the 72nd.
But the two-goal lead was restored six minutes later. Townsend picked up the ball near halfway line and ran through the defense before sending a swerving shot in off the right post.
Sturridge's penalty kick concluded the scoring.