Lee Carsley’s Young Lions had already sealed qualification for next summer’s showpiece in Georgia and Romania.
But they were hoping to end their Group G qualification campaign on a high at Huddersfield’s John Smith’s Stadium.
Instead, however, goals in either half saw Slovenia’s youngsters inflict a first qualifying defeat on England with Cameron Archer’s injury time strike not enough to prevent defeat.
Slovenia had got off to the perfect start when they took the lead just 45 seconds after kick-off.
Djed Spence inadvertently headed in past home ‘keeper Josef Bursik as he attempted to clear Luka Vesner Ticic’s free-kick.
And another set-piece saw Slovenia double their advantage on 65 minutes, Mark Zabukovnik heading home from a pinpoint Vesner Ticic free-kick.
England’s youngsters enjoyed plenty of territory and possession with Jacob Ramsey twice going close in the first half and Emile Smith-Rowe seeing a second half effort deflected wide.
And when Archer struck in injury time it set up a frantic finale but Slovenia held on to claim the three points.
It meant the Young Lions finished with eight wins, a draw and defeat from their overall qualifying campaign.
City’s Tommy Doyle and James McAtee were both unused substitutes.
