The captain's 59th-minute penalty, on the evening of his 100th appearance, was a 44th international goal that drew him level with Jimmy Greaves at third-place in the catalogue of England's all-time top goalscorers.
It also drew his side level on the night, barely two minutes after a Jordan Henderson own goal had put Slovenia in front, and paved the way for a fourth straight Group E victory secured by Danny Welbeck's double (66 and 72).
The result gives England a six-point cushion on Slovenia, who came to London in second place following back-to-back wins.
Only Gary Lineker and Sir Bobby Charlton now have more England goals than Rooney, meanwhile, and it was the World Cup-winning knight of the realm who presented the skipper with his commemorative golden cap before kick-off.
The dazzle of that piece of memorabilia was not matched by a subdued first half, England's patient but powder-puff attacks failing to force a single stop from Slovenia goalkeeper Samir Handanovic.
In fact, amid a series of off-target long-range shots from the home side, it was Slovenia who went closest to a goal as Milijove Novakovic flashed a near-post corner wide after wandering unguarded across the England box.
Set-pieces always appeared the likeliest route to goal for the visitors, and so it proved 12 minutes after half-time as Henderson, in his eagerness to defend a dangerous Novakovic delivery, skimmed a header past Joe Hart.
England were stung into action and won a penalty within 90 seconds as Bostjan Cesar, whose first-half forearm smash on Adam Lallana had been deemed accidental by the officials, needlessly nibbled at Rooney's ankles. The captain's spot-kick was too firm for Handanovic, who guessed right.
Shortly afterwards England were in front, Welbeck bobbling in a left-footed follow-up when Adam Lallana's deflected shot came back off Handanovic and fell obligingly.
And the Arsenal striker sealed a fifth successive victory — England's best run since 2008 — with the goal of the game, tucked wide of the Slovenia keeper after a smart give-and-go with Raheem Sterling.