Needing to beat American Taliyah Brooks by about six seconds to make the podium, Johnson-Thompson ran a season-best of 2:07.38 to finish second, with Brooks posting 2:13.17 in ninth.
Remarkably, after a lengthy delay, the race result saw Johnson-Thompson and Brooks locked on 6581 points as it was confirmed both athletes would share bronze.
Tears of joy soon flowed for 32-year-old Johnson-Thompson, who has now won medals at the last three major global competitions.
Anna Hall of the United States took gold with 6888 points as Ireland's Kate O'Connor claimed silver with 6714.
Speaking to BBC Sport, Johnson-Thompson said: “I have no words. I'm still in a bit of disbelief…the season’s been so difficult, I’ve done this so many times and it doesn’t get any easier. I think I had the least confidence coming into this.
“I don’t even think this is the hardest-fought medal I’ve got, but honestly, it really does mean the world to me.”
Johnson-Thompson’s medal is Loughborough University’s second of the World Championships following Jake Wightman’s silver on Wednesday.