In the territory of the current municipality of San Demetrio, the Italic people of the Vestini resided, more precisely, the Vestini Cismontani, who occupied the valley of the Aterno River.
The town was already known in the Middle Ages as "Pagus chrementes" and later as Demetra, but the toponym "San Demetrio" appeared in the 10th century in the Chronicon Farfense; at that time, it was not a unified fortified center but rather a collection of scattered villages: Cavantoni, Cardamone, Cardabello, Colle, Collarano, Villagrande, and Villa San Giovanni. In 1254, the castle of Sinizzo, in the territory of San Demetrio but now disappeared, participated as a founding castle in the foundation of L'Aquila, occupying a location in the Santa Giusta district.
San Demetrio was involved, like other centers in the area, in the war of L'Aquila, led by the Aragonese captain Braccio da Montone, who occupied the castle in 1423; only the nearby castle of Stiffe managed to resist the siege. After Braccio's defeat by the Angevins, San Demetrio sought autonomy by establishing the university; breaking away from the control of L'Aquila, it began to develop demographically and economically, particularly in cereal cultivation. During this time, bourgeois families such as Marimpietri, Cappa, Cappelli, and Visca prospered, and with the proceeds from shepherding and transhumance, they also moved to L'Aquila. In 1442, King Alfonso I of Aragon stayed in San Demetrio, coming to settle a territorial dispute between the town and L'Aquila.
In 1553, San Demetrio was enfeoffed to Captain Ferdinando Aguilera, and in 1691, the university asked the Kingdom to establish a public market every Friday, a tradition that continues to this day. In 1809, San Demetrio was granted the privilege of celebrating a special fair every year, and on July 5, 1862, when the town became part of the new Kingdom of Italy, it changed its name, identical to another municipality in Calabria, to "San Demetrio ne' Vestini," in memory of the ancient Italic people.
On April 6, 2009, the high province of L'Aquila was hit by a violent earthquake, causing three casualties and extensive damage in San Demetrio ne' Vestini. Among the most significant incidents were the collapses of the facade of the church of Santa Maria dei Raccomandati, the bell tower of the church of San Giovanni in the homonymous fraction, and the devastation of Lake Sinizzo.
