[2] Named for the original inhabitants of the area, the Menominee,[6] the city forms the core of the United States Census Bureau's Menomonie Micropolitan Statistical Area (MSA), which includes all of Dunn County (2020 population: 45,440).

The city center is at the south end of Lake Menomin, a reservoir on the Red Cedar River.

The earliest known residents of the area were people from the Trempealeau Hopewell Culture of the Middle Woodland Period (100–400 CE).

It is theorized that agricultural villages supported the population during summer months, transitioning to hunting and gathering from fall through spring.

The next known population group is the Santee Dakota in the 1600s and 1700s, who engaged in conflicts with the Ojibwe people, who migrated west as refugees.

Armed with European weapons, the Ojibwe pushed westward, eventually winning at the Battle of Kathio in 1770.

The two tribes continued their warfare, eventually signing the 1825 First Treaty of Prairie du Chien, which made a border between the two just north of Menomonie, with the Dakota claiming the southern lands.

[8] In 1788, French-Canadian fur trader and schoolmaster Jean Baptiste Perrault established a trading post and fort on the Red Cedar River very near Menomonie.

Hardin Perkins established the first sawmill at the confluence of Wilson Creek and the Red Cedar River in 1822 on behalf of fur traders James H. Lockwood and Joseph Rolette of Prairie du Chien.

Working with Indian Agent General Street, Perkins, Lockwood and Rolette began a legal battle over the authority of the local Native American people to grant permissions of this sort, exchanging land for payment of blankets, beads, whiskey, and other merchandise to Dakota Chief Wapasha II and other Ojibwe chiefs.

[8][10] Lockwood built a second mill and dam on the west side of the Red Cedar River, at the confluence of Gilbert Creek.

In 1839, Allen built a new sawmill in its place, which he sold to the McCann brothers, settlers from Ohio who later became the first permanent residents of Eau Claire.

[13] Lockwood and Rolette sold their original operation to James Green in 1841, who turned over the deed to William Black in 1842.

Wilson founded the city of Menomonie and became its first mayor in 1882, as well as a Wisconsin State Senator.

Tainter was a silent partner, whose duties included shipping lumber down to the Mississippi River and returning with supplies.

[10] The post office was moved to the site of the Knapp, Stout & Co. Company in 1855, with Wilson as postmaster.

In 1902, the Wilson-Weber Lumber Company took over retail operations of the Knapp, Stout & Co. That same year, Menomonie founded the nation's first agricultural high school, the Dunn County School of Agriculture and Domestic Economy.

These routes run as follows:[28] Menomonie Municipal Airport (KLUM) serves the city and surrounding communities.