Sunderland will play third tier football for only the second time in their history.
Perhaps unsurprisingly, the hammer blow was struck by Darren Bent, a late substitute for the visitors who kept their own faint hopes of surviving alive.
Sunderland looked to be heading for another win that would keep them just about in touch with the teams above them, but again they just could not hold on.
When Liam Boyce headed home a late winner, loud cries of 'Are you watching Ellis Short?' rang around the ground.
The Brewers celebrated wildly as the Black Cats rued yet another opportunity inexplicably missed.
They looked like they had rescued a late equaliser when Paddy McNair bundled the ball over the line, but it was ruled out for handball after the referee consulted his linesman.
The gap to Bolton Wanderers is now six points with two to play, but with Burton and Bolton still to face each other, hopes of survival are gone.
It was a sluggish contest that Sunderland should have seen out but again they could not do it.
Paddy McNair was the first to draw a meaningful save, striking on his weaker foot as he broke into the penalty box. It was a sweeping counter started by Lee Cattermole, teeing up Callum McManaman who drove infield before playing the ball inside for the Northern Irishman, who Chris Coleman has recently said is absolutely crucial to any rebuild.
Within ten minutes, he was on the scoresheet.
Ashley Fletcher did brilliantly, running towards goal and holding off the attentions of numerous Burton defenders. The ball looked lost but he recovered, moving the ball into the path of McNair. His drive from range was struck sweetly, but went straight through Steven Bywater who ought to have saved.
Sunderland were able to take their lead into the interval despite some late Burton pressure, with Joe Sbarra missing a glorious opportunity as he sliced Lukas Akins' cross wide at the back post.
The visitors started the second half much the better and Coleman was forced to act quickly when Marc Wilson put himself in danger. The Irishman had been booked for a late foul in the first half and took a risk when he was penalised near his own box. The Black Cats boss turned to Adam Matthews and shortly after Aiden McGeady fired wide with the host's first real attack of the half.
Burton's momentum had somewhat faded, but Jason Steele had to be alert to push Jacob Davenport's long-range free-kick wide of the post. Steele had been restored to the starting XI ahead of Lee Camp and showed some much-need assurance, roared on by the South Stand.
Sunderland ought to have put the game to bed with ten to play when substitute Joel Asoro ran clear on the left. Torn between shooting and cutting the ball back across goal, he could only find the Burton defender. Honeyman raced towards the loose ball but saw his effort cleared.
Desperate for an equaliser, Nigel Clough threw on Darren bent to a chorus of boos from the home support.
With just four minutes left to play, he headed home the goal that surely condemns Sunderland to the drop. Hope Akpan stung Steele's palms from range, with Bent reacting fastest to head home.
Sunderland nearly retook the lead when John O'Shea headed Aiden McGeady's free-kick onto the bar, with Jake Clarke-Salter turning the rebound wide.
Burton were ahead when Liam Boyce headed home a cross soon after, in what looked like the last meaningful action of the game.
Sunderland thought McNair had headed home a second but it was cruelly ruled out for handball.
Sunderland XI: Steele; Jones, Kone (Clarke-Salter, 81), O'Shea, Wilson (Matthews, 60); Cattermole, McNair, Honeyman; McManaman (Asoro, 65), McGeady, Fletcher
Subs: Camp, LuaLua, Maja, Ejaria
Burton Albion XI: Bywater; Brayford, Naylor, McFadzean, McRory (Turner, 60); Davenport, Akpan, Sbarra (Bent, 75), Akins, Murphy (Sordell, 81); Boyce
Subs: Campbell, Buxton, Allen, Samuelsen
Attendance: 25, 475
Bookings: Wilson, 44 Davenport, 45 McManaman, 59