Falerone is two towns, one above the other. In 29 before Christ, within the Augustan centuriation of the Tenna valley, Falerio Picenus was built, a junction between Firmum, Urbs Salvia and Asculum; its ruins, with the theatre of about sixteen hundred seats dug out in 1838, lie two kilometres from the medieval village, down at Piane di Falerone. In Domitian's time the people of Falerio and those of Fermo went to law over land the triumvirs had taken from the Fermo territory and never given back; the emperor decided for Falerio, and the bronze copy of his rescript was found at Falerone. In 765 the town was the seat of a Lombard gastaldate under the duchy of Fermo.
From 977 the lords of Falerone, vicars of Farfa and convinced Ghibellines, held the neighbouring castles as well, until 1378, when Stefano and Vanni, sons of Pietro II, were sentenced by the Council of Fermo to leave Falerone and live in the city, for killing Berto, son of the lord of Massa Fermana, in a brawl that broke out during a local feast. Fermo used that sentence as a pretext to uproot the lordship and occupy the town. In May 1418 Braccio da Montone stormed the fortress to catch Lodovico Migliorati, lord of Fermo, who had taken refuge in it: he sacked the place, imprisoned the inhabitants, destroyed the community's historical archive and demanded nine thousand ducats to ransom his prisoners. In 1520 Ludovico Euffreducci, a descendant of those lords, came back with two hundred horse and two thousand foot and was killed in the Tenna valley by Giovanni de' Medici's men; his partisans took shelter in Venice and Romagna, and returned later under a changed surname, Emiliani.