The town was already Vetus Doadum ("Old Doadum"), Teotuadum castrum, in Late Antiquity, identifiable in a document of 631 as Castrum Doe. The foundations of a 6th-century circular baptistery beside the natural springs has been uncovered beneath the ruins of the pre-Romanesque church of Saint-Léger, itself destroyed in the 17th century. It was the site of a Gallo-Roman villa that was inherited by the Carolingians. In his villa here, Theoduadum palatium, Louis the Pious was informed of the death of his father Charlemagne in 814 and hurried to Aachen to be crowned. The villa was turned into a motte in the 10th century, around which the village developed, in part in excavated troglodyte dwellings. In 1055 the site was identified as Doedus, then Docium in 1177.

Doué-la-Fontaine is the site of the oldest habitable donjon (keep) in France, dating back to the year 900. No traces of Doué's medieval fortifications remains, save the names of "gates" given to certain streets. The castle is widely believed to have been the first European castle to be built out of stone (at around 950).

Nearby are the troglodyte dwellings, where the inhabitants took refuges from the Normans, and commercial mushroom-growing caves. The stone of Doué-la-Fontaine was quarried for sarcophagi 4 km (2.5 mi) from the town. The Zoo of Doué-la-Fontaine is partly built within the network of the troglodytes sites and dwellings. Recently, a cave containing sarcophagi was unearthed.

In 1793, Doué-la-Fontaine was the site of massacres during the counter-Revolutionary Revolt in the Vendée, suppressed by General Santerre.

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