He was elected to succeed his friend Andrew Jackson as a member of the Tennessee Supreme Court in 1804, where he served as a judge until 1810.

In 1819, he founded Memphis, Tennessee on land he owned with Andrew Jackson and James Winchester.

The nearby John Overton Comprehensive High School, located just across the railroad tracks that abut the property, is named in his honor.

The Overton Lodge of Free and Accepted Masons on the historic courthouse square in Rogersville, Tennessee was named after John Overton and is the oldest continuously operating Masonic lodge in the state of Tennessee, and has been operating from the same building since circa 1840, and is a contributing property to the Rogersville Historic District.

Perkins Baxter Overton grew up playing on the Travelers Rest grounds and is the great-great-great-grandson of Judge John.