The game looked to be petering out into a tame draw but Smith, brought on with just four minutes remaining, rose at the back post and powered the ball past Dillon Phillips to earn the hosts all three points.
Charlton have still not beaten Millwall in the league since 1996, when manager Lee Bowyer, then a teenager, was on the scoresheet.
And the visitors did not look like they had any hope of ending that run in the first 20 minutes, during which they were utterly overrun.
In an electric atmosphere at the Den, Millwall made a lightning-fast start, and almost took the lead after just four minutes, when Phillips flapped at a deflected cross which dropped for Jed Wallace, only for his powerful strike to be blocked.
Charlton's reprieve lasted only two minutes though, as the home side's early pressure paid off from a free-kick.
Shaun Williams crossed from the right and somehow Hutchinson was left unmarked eight yards out to steer his header home.
Millwall then almost doubled their advantage after just nine minutes, with full-back Mahlon Romeo getting forward and unleashing a powerful drive from the edge of the box which forced Phillips into a good save.
But the visitors began to get a foothold in the game as the first half wore on, and went close twice.
The Millwall keeper then redeemed himself with a stunning save in first-half stoppage time, pushing Macauley Bonne's close-range volley over the bar.
Bialkowski was called into action again soon after half-time, this time pushing a Darren Pratley effort over, but from the resulting corner he was finally beaten.
After the first ball had been cleared, Charlton worked it back into the box where Leko was able to place his volley into the corner.
As the minutes ticked by it seemed both sides were more concerned with avoiding defeat than chasing a winner.
That was until seconds from the end when Smith bullied his defender out of the way and headed the winner, sending the home fans delirious.