Castiglione del Lago has evolved on what used to be an island - the fourth island of Lake Trasimeno, in its south west region. Over the centuries, as the town grew, the flat gap between the island and the shore was filled with piazzas, houses, churches and other buildings.

The newest parts of the city are at some distance from the old, so the centro storico (historical center) of Castiglione del Lago is a well-preserved medieval locality that seems to be governed by a "law of threes". In the town walls there are three gates, and inside the town there are three piazzas and three churches.

The Fortress of the Lion was built by Emperor Frederick II. The pentagonal-shaped castle, was completed in 1247 CE by the monk-architect Elia from Cortona. The castle features square towers in four of its corners and a triangular shaped bastion, or donjon, known as the Mastio in the other. The castle was designed to give its owners strategic control over all of Lake Trasimeno. The castle has withstood a number of sieges over the subsequent centuries.

The Palazzo della Corgna which serves as the Palazzo del Comune (Town Hall) was built by Ascanio della Corgna in Renaissance style, designed by the architect Vignola. It is now a civic museum and gallery. The palazzo has by a long, covered corridor connecting to the castle. On the main floor, late Renaissance era frescoes were painted by the Pescaro-born artist Giovanni Antonio Pandolfi and the Florentine artist Salvio Savini. In 1574, the artist Niccolò Circignani, known as "Il Pomarancio", added paintings and other decorations to one of the most interesting rooms in the palazzo, the so-called Room of the Exploits of the overlord Ascanio della Corgna.

The only other building of particular note is the finely stucco-ed Church of Santa Maria Maddalena, done on a Greek-cross plan. The church has a neo-classical pronaos and, inside, a panel painted in 1580 by Eusebio da San Giorgio.