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Atherstone has a long history dating back to Roman times. An important defended Roman settlement named Manduessedum existed at Mancetter near the site of modern-day Atherstone, and the Roman road, the Watling Street (now known as the A5) ran through the town. It is believed by some historians that the rebel Queen of the Britons, Boudica, was defeated at the Battle of Watling Street by the Romans in her final battle near Manduessedum.

The Domesday Book of 1086, records that Atherstone was held by Countess Godiva.

The ancient St. Mary's Chapel in Atherstone dates from the early 12th century when the monks of Bec made a donation of 12 acres (4.9 ha) to a house of friars and hermits, later referred to as "Austin friars". According to Nichols, the chapel was granted to Henry Cartwright in 1542, then left abandoned and neglected until 1692 when Samuel Bracebridge settled a yearly sum for the parson of Mancetter to preach there every other Sunday in the winter season.

After this, St. Mary's Chapel seems to have experienced something of a revival. Its square tower being rebuilt in the fashionable "Gothic" style in 1782. This drastic alteration probably aroused some controversy. although the fine architectural drawing of the chapel made by Mr. Schnebbelie in 1790 prompted Nichols to assert that "the new tower provides a good effect". St Mary's was further redesigned in 1849 by Thomas Henry Wyatt and David Brandon.

It is said that the Battle of Bosworth actually took place in the fields of Merevale above Atherstone. Certainly reparation was made to Atherstone after the battle and not to Market Bosworth.

In Tudor times, Atherstone was a thriving commercial centre for weaving and clothmaking. The town's favourable location laid out as a long 'ribbon development' along Watling Street, ensured its growth as a market town. While it remained an agricultural settlement in medieval times, attempts were made to encourage merchants and traders through the creation of burgage plots, a type of land tenure that provided them with special privileges. A manuscript discovered by Marjorie Morgan among the muniments of Cambridge’s King's College (Ms. C9), refers to the creation of nine new burgage strips from land belonging to seven of the tenants in Atherstone vill.

By the late Tudor period Atherstone had become a centre for leatherworking, clothmaking, metalworking and brewing. Local sheep farmers and cattle graziers supplied wool and leather to local tanners and shoemakers (an industry that continued until the 1970s), while metalworkers, locksmiths and nailers fired their furnaces with local coal and the alemakers supplied thirsty palates on market days.

The surviving inventories from 16th century Mancetter provide a fascinating glimpse into Atherstone’s Elizabethan merchants and traders, before the town was economically overshadowed by the bustling cities of Coventry and Birmingham. They show Atherstone at this time as a typical Midlands market town, taking full advantage of its location and agricultural setting.