On the night artist Anna Weyant’s work debuted at Christie’s, the 27-year-old painter was too nervous to attend or even watch the livestream. Instead, Ms. Weyant holed up in her small Manhattan apartment and listened to a calming app on her cellphone until a friend texted with news. 

“Summertime,” Ms. Weyant’s portrait of a woman with long, flowing hair that the artist had sold for around $12,000 two years before, resold for $1.5 million, five times its high estimate.

It has been a rocket-fueled rise to the top of the contemporary art world for Ms. Weyant—and far from her unassuming start in Calgary, Canada. Spotted on Instagram three years ago and quickly vouched for by a savvy handful of artists, dealers and advisers, Ms. Weyant is now internationally coveted for her paintings of vulnerable girls and mischievous women in sharply lit, old-master hues.