The team plays its home matches at Energizer Park, a soccer-specific stadium across from Union Station in Downtown West.

[5] Despite approved plans to build the $600 million Collinsville Soccer Complex, MLS was unimpressed with the bid's financial backing and suggested Cooper expand his group of investors.

[13] The proposed ownership group sought public funds to help build a $200 million soccer-specific stadium next to Union Station in downtown St. Louis.

[16] St. Louis's MLS bid was effectively re-launched on October 9 of that year, with Carolyn Kindle and other heirs to the Enterprise Rent-A-Car fortune as the primary investors.

[18] On November 28, 2018, the Board of Aldermen's Housing, Urban Development, and Zoning Committee voted 8–0 to approve the stadium plan.

The league, currently at 27 teams, advised the Commissioner's office to advance the discussions with the Sacramento Republic and St. Louis bids.

Both bids were asked to make presentations to the MLS Expansion Committee to "address each bid's final stadium plan, corporate commitments, the composition of the respective ownership groups, detailed economics on funding, strategic plans for fan development, commitments on player development and details on community programs.

[24] In the announcement, Don Garber said, "St. Louis is a city with a rich soccer tradition, and it is a market we have considered since the league's inception.

Our league becomes stronger today with the addition of the city's deeply dedicated soccer fans, and the committed and innovative local ownership group led by Carolyn Kindle Betz, the Taylor family, and Jim Kavanaugh.

They also set a new record as the 3rd team to have 15 points in its first five games, joining the Los Angeles Galaxy in 1996 and Sporting Kansas City in 2012.

[35] On April 1, 2023, St. Louis City SC lost their first game in their history against Minnesota United FC with the score 0–1 in CityPark.

[38] On October 1, 2023, St. Louis City SC won the Western Conference in their first year as a franchise and would also qualify for the 2024 CONCACAF Champions Cup.

On November 5, 2023, St. Louis was eliminated from the MLS Cup Playoffs after being swept by Sporting Kansas City in the first round best-of-three series.

Officially, the team's colors are city red, river blue, energy yellow, arch steel gray, and white.

[43][44] The stadium is intended to field 17 to 23 soccer games a year and serve as a venue for concerts, high school sports, and more.

The St. Louligans were founded in 2010 when several local soccer fan groups joined forces at AC St. Louis home games.

Notable contributions of the group include awarding a new fan each week with a ticket, and coordinating with the Coopers, supporters for Louisville City FC, to create the Kings' Cup rivalry competition between the two teams.

For their first encounters in 2023, the two teams met twice in the space of a week, and Chicago won both matches despite their visitors sending large numbers of traveling supporters.

A series of emails from Sporting Kansas City’s front office arrived in the inbox of the podcast’s Gmail account.

In August 2020, the club announced the founding of the St. Louis City SC Academy, joining MLS Next in the 2020-21 season.

[78] On August 26, 2022, the UPSL announced that St. Louis City SC has joined the league, and will compete in the KY / TN Conference - Premier Division.