According to the legend, said to have been recorded around 1330 BC by a mythological Quirinus Colonus, Todi was built by Hercules, who here killed Cacus, and gave the city the name of Eclis.
Historical Todi was founded by the ancient Italic people of the Umbri, in the 8th-7th century BC, with the name of Tutere. The name means "border", being the city located on the frontier with the Etruscan dominions. It probably was still under the latter's influence when it was conquered by the Romans in 217 BC. According to Silius Italicus, it had a double line of walls that stopped Hannibal himself after his victory at the Trasimeno. In most Latin texts, the name of the town took the form Tuder.
Christianity spread to Todi very early, through the efforts of St. Terentianus. Bishop St. Fortunatus became the patron saint of the city for his heroic defense of it during the Gothic siege. In Lombard times, Todi was part of the Duchy of Spoleto.
After the 12th century the city started to expand again: the government was held first by consuls, and then by podestà and a people's captain, some of whom achieved wide fame. In 1244 the new quarters, housing mainly the new artisan classes, were enclosed in a new circle of walls. In 1290 the city had 40,000 inhabitants. Communal autonomy was lost in 1367 when the city was annexed to the Papal States: the local overlordship shifted among various families (the Tomacelli, the Malatesta, Braccio da Montone, Francesco Sforza and others). Although reduced to half of its former population, Todi lived a brief period of splendour under bishop Angelo Cesi, who rebuilt several edifices or added new ones, like the Cesia Fountain that still bears his name.
In July 1849 Todi received Giuseppe Garibaldi, who was fleeing after the failed democratic attempt of the Republic of Rome.
Todi is the birthplace of the Franciscan poet Jacopone da Todi, who is buried in a special crypt in the church of S. Fortunato