St Louis will join Major League Soccer in 2022 and become MLS' first club to have a female-led ownership group.
The league currently has 24 teams but has announced plans to expand to 30 - David Beckham's Inter Miami CF and Nashville join next season, Austin FC in 2021 and St Louis a year later.
"St Louis is a city with a rich soccer tradition," said MLS chief Don Garber.
"It is a market we have considered since the league's inception. It is with great pride we welcome St Louis."
To become the 28th franchise, the team behind the St Louis bid had to pay a $200m (£165m) expansion fee.
Led by members of the founding family of car rental company Enterprise, the new club joins the Stanley Cup ice hockey champions St Louis Blues and 11-time World Series baseball champions Cardinals as the city's major sports teams.
Enterprise president Carolyn Kindle Betz said: "It's an incredible feeling to now be able to say St Louis is home to the first official majority female-led ownership group in MLS.
"Our MLS team and stadium will only add to St Louis' renaissance currently underway and will provide us with a great opportunity to bring together many different segments of the community, uniting people in their love for the game."
The league, which operates East and West Conferences, announced its plan to expand to 30 teams in April. The 29th franchise will pay the same entry fee as St Louis, with the entry requirements for the final place yet to be announced.