Slovenia were on track to advancing despite being down 1:0 on a 23rd minute goal by Jermain Defoe. But Landon Donovan scored in the last minute for the US, shattering Slovenia's hopes of achieving the biggest success in national football history.
Both teams looked nervous at the start but quite equal until Frank Lampard warmed up keeper Samir Handanovic with a shot from 35 metres in the 14th minute, a move that signaled the start of English dominance.
Defoe turned the game around in the 23rd minute, when he converted James Milner's cross from five meters with a right-foot volley that would prove to be England's ticket to the top 16.
Dafoe and Frank Lampard were close to taking England to a two-goal lead in the 26th, but Dafoe's shot was deflected by Miso Brecko and Lampard's went wide.
England had several serious opportunities early in the second half as Slovenian defence crumbled. Defoe had a chance in the opening minute of the second half, but he flicked the ball wide.
Keeper Handanovic was kept very busy, blocking John Terry's header in the 57th minute and finger-tipping Wayne Rooney's shot into the post a minute later.
In the 68th Slovenia were within a whisker of equalising, but amidst confusion in England's penalty area consecutive shots by Milivoje Novakovic, Zlatko Dedic and Valter Birsa failed to land in the net.
The pace slowed down in the final twenty minutes, with both teams still on track to making it to the next round as Algeria held the US to a goalless draw.
But in overtime Landon Donovan scored for the US, securing a last-minute ticket to the round of 16.
Slovenian players were clearly disappointed at the outcome. "If we had more experience we could have won this game. We're disappointed, but we're proud of our four points and proud of being a real team," Robert Koren said.
But coach Matjaz Kek did not share the players' disappointment, on the contrary he said he was "proud and glad to be in the company of these boys, to have done what we have done."
"We had the match ball at the end and could have gotten that golden point, but this is just how things are in sport. If you cannot be big in defeat...you don't deserve victory," said Kek, who hopes England will get "to the end" at the World Cup.
The US ended the preliminary round at the top of Group C with five points. England have five points as well but scored fewer goals and Slovenia are in third with four points from a win against Algeria and a draw with the US.
Despite the bitter aftertaste, the South Africa campaign will go down in history as Slovenia's most successful bid yet at a major international tournament.
In their first stint at Euro 2000 Slovenia managed a sole draw with Yugoslavia. It walked away without a single point from the 2002 World Cup in Japan and South Korea.