Prairie Commons had its beginnings with the purchase of a 4.3 acre site on Utz Lane, between Howdershell Road and Dunn Road, in what is now the City of Hazelwood. On September 15, 1986, the Branch opened its doors to serve the northwest area of St. Louis County, including Hazelwood and part of Florissant.

Naming the branch caused a flurry. "Possum Hollow" emerged as a possibility, which was what locals called this historical area. This was not, as it turned out, a universally popular choice. "Hazelwood Grateful for Library, Ungrateful for Name," was the headline of an article on the new Branch in the St. Louis Post-Dispatch. "No one liked the name. They didn't think the name was dignified," Hazelwood City Clerk had voiced the general consensus in the article. In the end, "Prairie Commons" was chosen because the surrounding area had once been part of the prairie and the building stood on what had been St. Ferdinand Commons in the days of the French Settlement.
People come to the branch because they notice it from Interstate-270. In June of 1991, a very visible sign was erected on the I-270 side of the building and a noticeable increase in circulation followed.