Originally known as the Linn County Bridge, this bridge is the longest of the four surviving covered bridges in the state. The Howe-truss bridge was built in 1868 and features arched entrances with ramps sloping away from both ends. A foot bridge makes the bridge accessible to visitors.

On August 4, 1868, the Linn County Commissioners awarded a contract to the firm of Bishop & Eaton for construction of a covered bridge at a cost "not to exceed $5,000." The  151 foot structure, orignally known as the linn County Bridge, was completed and opened to traffic the same year. It is the longest of the four surviving covered bridges in the state.

The bridge was built with the Howe-truss system and features arched entrances with ramps sloping away from both ends. It was situated on the main east-west road in northern Missouri, running parallel to the Hannibal and St. Joseph Railroad. Midway between Laclede and Meadville, Locust Creek Covered Bridge served a local population that included the young John Joseph Pershing, who became the nation's highest ranking military commander. As a boy, Pershing swam and fished in the creek near the bridge.

The road on which the bridge was located later became Route 8, the nation's first transcontinental highway. Locust Creek's channel was altered following World War II, leaving the bridge spanning a dry creek bed, and Us. Highway 36 replaced Route 8 as the main traffice artery across northern Missouri. By 1960, the county ahd ceased maintaining of the west access road, and the bridge became virtually inaccessible. The state of Missouri received title to the bridge in 1968 and designated it a state historic site. Two years later it was placed on the National Register of Historic Places.