Bolt took the baton for Jamaica in third place but within a few strides he had fallen to the ground, clutching his left leg, as host Britain secured a shock gold ahead of a United States team containing Justin Gatlin.
Bolt beaten into third in the individual 100m behind Gatlin and his US team compatriot Christian Coleman, was comforted by teammates after getting to his feet.
The capacity crowd in the London Stadium was still digesting the shock earlier defeat for home hero Mo Farah in the men’s 5,000m final, before the drama of Bolt’s last agonizing appearance.
He had been bidding for a 12th world championship gold to bring down the curtain on his glittering career, but left the arena accompanied by medical staff and a wheelchair.
Victory for the British quartet of CJ Ujah, Adam Gemili, who ran a storming second leg, Daniel Talbot and Nethaneel Mitchell-Blake was stunning compensation for Farah’s earlier defeat. They won in 37.47 seconds, with the US taking silver at 0.05sec and Japan with a surprise bronze.
Farah bows out with silver
Farah, who won the 10,000 title in dramatic fashion of the opening day at the London Stadium, had to settle for silver behind Ethiopian Muktar Edris in his final championship race on the track.
He edged out American Paul Chelimo in a desperate dash for the line, the last mile of a hitherto slow run race run in just under four minutes.
Farah, 34, will now turn his attention to the marathon after failing in his bid to double up at the Olympics or World Championship for the fifth time, including double gold in London 2012 and the Rio Games last year.
Edris, a former world junior champion, timed his last lap burst to perfection to win in 13 minutes 32.79 seconds, copying Farah’s famous Mobot gesture as he crossed the line.
It was not the farewell Farah wanted, but he pointed to his earlier exertions in a dramatic 10,000m final as reason for lacking his usual devastating finish.
“The 10,000m took a lot more out of me than I had realized,” he told BBC Sport.
“I gave it my all. I didn’t have a single thing left to give at the end.”