The Jamaican was just 0.05 seconds off Florence Griffith Joyner’s mark of 10.49 seconds in 1988.
The Jamaican blazed to victory at the Prefontaine Classic in 10.54secs, eclipsing the 10.61s she ran to defend her Olympic title in Tokyo last month.
She finished well clear of compatriot Shelly-Ann Fraser-Pryce who clocked 10.73.
Griffith Joyner’s mark of 10.49 from 1988 has long appeared untouchable, but Thompson-Herah’s exploits this summer have brought it within reach for the first time in a generation.
“To come back with a personal best after the championships, that is amazing,” said the 29-year-old, who also won 200m and 4x100m gold in Tokyo.
“I have more races, so I don’t get too excited, too carried away. I have to continue doing the job.”
Sha’Carri Richardson, the American who missed the Olympics after testing positive for cannabis, finished last in 11.14 in her first race back following a one-month ban.
The 21-year-old, whose 10.72 from April makes her the sixth fastest woman in history, was typically defiant afterwards, saying: “I wanted to be able to come and perform after having a month off and dealing with all I was dealing with. I’m not upset with myself at all.
“This is one race. I’m not done. You know what I am capable of. Count me out if you want to. Talk all the s*** you want, because I’m here to stay.”
Dina Asher-Smith whose 100m and 200m medal hopes in Tokyo were dashed by a hamstring injury, clocked 22.19 to finish third in the 200m, while Olympic silver medallists Laura Muir and Keely Hodgkinson were 12th and fifth in the 1500m and 800m respectively.