After winning their last 14 qualifying matches, England were denied three points for the first time on the road to a major tournament since 2013.
For so long the main man for club and country, Rooney's recent slump had seen him dropped by United and then England in the space of a few weeks.
Whatever Rooney's failings of late, it was still a bold move from Southgate and the pressure was on Eric Dier and Dele Alli to prove he was right to put his faith in the Tottenham duo ahead of such a vastly experienced star.
Alli, the man who has taken the number 10 role from Rooney, nearly conjured an early goal when his astute pass sent Daniel Sturridge through on goal, but Slovenia goalkeeper Jan Oblak was quick off his line to block.
Dier, the other player Southgate preferred to Rooney in midfield, made a less accomplished start as he attempted a backpass without looking and Slovenia striker Roman Bezjak pounced to surge clear for a shot that Hart saved well.
England still couldn't clear the danger and Jasmin Kurtic had time and space to set himself for a curling shot that beat Hart, only to rebound off the far post to Bezjak, who scuffed wide with the goal at his mercy.
Southgate's men were struggling to find any rhythm and finished the half without a shot on target.
There was no sign of any improvement from England after the interval and Hart, enjoying his best display since being exiled by Manchester City, had to scramble across to keep out Bostjan Cesar's close-range effort from a corner.
It took an even better stop from Hart to keep England level as he leapt to his left to push Kurtic's header onto the bar and then clawed the ball away again when it threatened to drop into the net.
Another piece of sloppy play from Dier gave Josip Ilicic a shooting chance and he was only just off-target from the edge of the area.
Southgate's first response to England's slumbering display wasn't to turn to Rooney and instead he sent on Crystal Palace winger Andros Townsend, who quickly forced Oblak to save.
Slovenia are 67th in FIFA's world rankings, but they were giving England fits and Hart had to come to the rescue again, saving from Ilicic after a dreadful backpass from Jordan Henderson.
With England's fans chanting Rooney's name, he replaced Alli in the 72nd minute and immediately reclaimed the captain's armband from Henderson.
Rooney almost made a dramatic impact when he whipped his first shot just past the post.
A Rooney lay-off gave Jesse Lingard a sight of goal in the closing stages, but Oblak made the save to deny England what would have been an undeserved success.
