Rooney marked the milestone with his 44th international goal, drawing alongside Jimmy Greaves at third in the list of England's top goalscorers, and his penalty levelled the game at 1-1 following a Jordan Henderson own goal.
Danny Welbeck then scored twice to maintain England's 100 per cent record in Group E of the European Qualifiers.
"It's a great feeling," said Rooney, who was presented with a golden cap by Sir Bobby Charlton before kick-off. "It was a big week and a great occasion - it's something I'm really proud of to walk out as captain with my two boys on my 100th game. I'll remember it for the rest of my life."
England manager Roy Hodgson was delighted to see Rooney celebrate the landmark with the crucial goal as he paid his own tribute.
"It was a wonderful evening for him," said Hodgson. "He's very important to me and to English football.
"It was fitting tonight he was able to really get his reward on the night when it's all about him. He picks up the cap, but also scores the important first goal and leads England to victory. We're delighted for him."
Rooney revealed Hodgson had warned his players to expect a frustrating night against visitors who came to London on the back of successive wins.
He told Sky Sports News HQ: "We actually worked on that through the week - we know Slovenia make it tough for teams and we expected that's how the game would go.
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"The second half was better - we created some good chances, especially when we went a goal down, and I thought we fully deserved the three points."
Rooney and Welbeck now have eight goals between them in qualifying, and the Manchester United man said of his former club-mate: "We're forming a great partnership. We know each other's games well, we've played together for United and I think that's showing.
"Danny's a fantastic player - we've all known that for years at United. Now he's got his move to Arsenal and he's playing and i think you've seen the beneftis of that with England."