Vonn skied immediately after Shiffrin pipped Olympic downhill champion Sofia Goggia for the lead.
And the 34-year-old, who last week announced her retirement after these World Championships, lost control on the top section and flew through a gate before crashing into the safety netting.
Shiffrin and Goggia were visibly upset after Vonn's incident but, after a worrying few minutes, the 2010 Olympic downhill gold medallist managed to ski down the slope to warm applause from the Swedish crowd.
Goggia held on for silver with Switzerland's Corinne Suter taking the bronze.
Vonn told NBC Sports that she will skip downhill training for the next two days and race in the downhill part of Friday's combined before lining up for Sunday's downhill proper.
"I was charging. I wanted to lay it all on the line. I didn’t see the piece of terrain exactly how I should have and my skis hooked up and I went straight through the panel. Just gonna be really sore the next couple of days.
"I'm too old to be crashing that hard. It’s like my body is not doing what my mind is telling it to do anymore." - Lindsey Vonn speaking to NBC Sports after her crash
Skiing third, Goggia set the pace on a shortened course with the start lowered due to high winds.
In her third race back from an ankle fracture, the Italian was a little untidy on the way down but her time of 1:04.91 proved hard to beat.
Suter was next to go and finished just three-hundredths of a second outside Goggia's time.
After Lara Gut-Behrami and defending champion Nicole Schmidhofer failed to trouble the front two, Goggia's team-mate Nadia Fanchini moved into third place.
The lead looked vulnerable, and it was finally taken by Shiffrin.
The 23-year-old is best known for her technical prowess but she currently leads the World Cup Super-G standings as well as the slalom and giant slalom series.
And despite almost missing a gate late on, she beat Goggia's time by just two-hundredths of a second to take her fourth World Championship gold medal.
The skies darkened following the delay after Vonn's crash which made conditions more difficult for the later competitors.
Vancouver 2010 giant slalom gold medallist Viktoria Rebensburg threatened the leaders but she finished fourth, just seven-hundredths off the lead and two-hundredths outside the medals.
Just 0.56 seconds separated the top 10 with Shiffrin saying, "It's hard to exactly put into words how this day felt. This is crazy. I really wasn't expecting this. It was a really tight race, the differences were like nothing.
"It was a fight. It's tough, all these girls deserved to win."
Shiffrin's fourth world title drew her level with childhood hero Bode Miller who was quick to congratulate his former team-mate.
Ted Ligety (five) is now the only American with more world titles than Shiffrin.
The days ahead
And Vonn? She is hoping her body recovers in time to end her career in Sunday's downhill.
Shiffrin has a decision to make too - whether to compete in the combined or concentrate on the slalom and giant slalom at the tail end of next week.
The American is aiming for a fourth consecutive world slalom title, and bidding to go one better than her giant slalom silver from St Moritz in 2017.