Originally known as "Jay Flat", it was established 2 miles (3 km) northeast of its present location and named after a local ranching family.

In 1907, the townsite was moved to its present location for improved proximity to rail service, and it was officially renamed "Jayton" later that same year.

The community's first newspaper, the Jayton Herald, was established the following year, and the city incorporated in February 1910.

From the community's inception, the local economy had originally been supported mainly by the cotton industry, but the Dust Bowl of the 1930s had a dire effect on production.

The community's economy was stabilized by the discovery of oil later that same decade, and while its population never exceeded 750, Jayton remained stable throughout the Great Depression.

In 1954, following a lengthy and heated court battle, the city wrested the title of county seat from the declining nearby community of Clairemont, and in 1957, a courthouse was constructed.

Texas State Highway 70 is Jayton's Main Street and leads northwest 24 miles (39 km) to Spur.

According to the United States Census Bureau, Jayton has a total area of 1.7 square miles (4.4 km2), all land.