The 22-year-old, the Olympic slalom champion and winner of the last three slalom World Championships, bagged her first speed win a day after claiming her first downhill podium place on the same course.
Shiffrin triumphed in one minute 27.55 seconds to beat Germany's Viktoria Rebensburg by 0.13 seconds with Switzerland's Michelle Gisin (1:27.72) third.
Lindsey Vonn, who crashed in Friday's Lake Louise downhill, skied with a brace on her right knee and finished tied 12th.
Shiffrin, the World Cup overall winner last season, was competing in just her fourth World Cup downhill race. Of her previous 32 World Cup wins, 26 have come in slalom.
The start was delayed by more than an hour because of a power outage, meaning racers had to ride snowcats or be towed to the top of a shortened course.
"Shortening the distance was definitely an advantage to me because the top section it's flat and I'm not as good up there," she told the FIS Alpine website.
'But from where we started most of the way down it's fairly technical and I felt really good about that yesterday so I took even a little bit more risk today and it paid off, just barely. But I also had really good light and some of those other girls had fog and it was really dark.
"I definitely know I was lucky today and yesterday but I skied well and I took some risk and it was fun."
Shiffrin's growing prowess at the speed events suggests there is a chance she might add these to her schedule at the Winter Olympics in South Korea in February.
"It's not a 100% 'no' but skiing in five events is maybe a little bit ambitious," she added. "My priority is slalom and giant slalom then the combined then downhill and super-G. Long story short, probably no."
Rebensburg won the first two giant slalom races of the season, while Gisin clinched only her second ever World Cup podium spot and first in downhill.
The women will contest a super-G on the same mountain Sunday.
On the men's circuit, Norway's Aksel Lund Svindal triumphed in the Beaver Creek downhill after missing most of last season following knee surgery.
Svindal, the 2010 Olympic super-G champion, tied for sixth in Friday's super-G but laid down an impressive time from start No.1 to beat Switzerland's Beat Feuz, who won the downhill opener in Lake Louise last week.
German Thomas Dressen claimed his maiden World Cup podium with third place at Beaver Creek.
It was Svindal's 13th downhill triumph and 33rd World Cup victory, the first since he won the super-G in Kitzbuehel in January 2016.
"I haven't won a race in a while so it was nice to feel the excitement of being in the leader box again," Svindal told reporters.
The men will race a giant slalom Sunday, but Svindal will not take part.
"My knee obviously works because I can race but it doesn't work perfectly," he said. "So I've had to make some tough decisions in training because I can only ski a certain amount a day."