The existing Šibenik Theatre is the successor to the Šibenik National Theatre, founded on 9 May 1945, home of a professional drama ensemble that performed until 1964, and an operetta ensemble that performed from 1946 to 1956. On 1 March 1966, the Šibenik Theatre (or Culture Centre, as it was known at the time) incorporated the Šibenik Children’s Festival, first held in 1958, which became the International Children's Festival in Šibenik.

Today, the Šibenik Theatre occupies a grand structure built in 1870, which makes it the second oldest theatre in Croatia. It was designed by architect Josip Slade from Trogir. It is the first and only theatre building in Croatia that was not built by the government, but by 28 shareholders, all citizens of Šibenik. A special addition to this grand building is its ceiling painted by artist Antun Zuccaro from Trieste with an allegorical depiction of famous citizens of Šibenik – Nikola Tommaseo, Antun Vrančić, Faust Vrančić, Martin Kolunić Rota, and Andrija Medulić, and among them a woman symbolising the region of Dalmatia, leaning on a stone crest.

After sustaining damage in the Croatian War of Independence in the 1990s, the building was completely renovated, and currently seats 310 people.