The first settlers were from Tennessee and Georgia, veterans of Creek Indian War of 1813 and 1814. The town was named for John Ash, a senator in the state's first General Assembly. In 1817, he was the first white settler to arrive. The log home that John Ash and Thomas Newton (his father-in-law) built in the center of the city, still stands as the oldest house in the county.
Ashville was incorporated in 1822 and served as the county's only courthouse until 1907. The first courthouse, which was made with logs, was built in 1824. The present courthouse was constructed in 1844. Ashville Academy, established in 1831, served as a meeting house for different church denominations.
The Methodists constructed a building to serve as both church and Masonic Lodge in the 1850s. By 1892, ownership had been transferred to the Masons. The building, that was moved twice, has been restored and currently houses the Mattie Lou Teague Crow Museum. It stands behind the John W. Inzer Museum, commemorating a Confederate officer from Ashville.
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