The oldest settlements date back to the 5th millennium BC. The data is affirmed by archaeological discoveries from the top of the hill (castle hill) at an elevation of 634 meters. The second period of settlements began in the second half of the 3rd millennium BC on nearby slopes of Drevenik. Lives of two cultures flourished there. The settlement ceased in the 2nd century AC. In the 11th century AC people moved to Drevenik where a fortified settlement emerged. People settled again on the castle hill during times of Hungarian state formation. Around the turn of the 11th and 12th century the castle hill was settled permanently. The beginnings of building the construction complex of the Spis Castle date back to that period of time.
Small settlements emerged in the surroundings of the castle as a centre of Spis. They were dependent on the castle. The inhabitants of the settlements were castle servants. Some of the settlements in question merged into villages or towns. The town of Spisske Podhradie arose by the connection of three settlements on the confluence of the brook of Jablonov and the brook called Teledin (later renamed - Carbon brook).
The first written mention of the town of Spisske Podhradie dates back to 1249. The document of king Belo IV that was addressed to Spis provost in the Spis Chapter House mentions a term “Villa Saxorum sub Castro” meaning “the settlement of Saxons under the castle”. The town that was independent of the castle arose by the mid - 13th century.
The town is well-known thanks to German immigrants and later it became the member of Community of Spis Saxons. Thanks to Saxons the guilds were created. The oldest one is linen guild established in 1385. In 1677 there were 16 official guilds, e.g. smith´s, beer-brewing, cabinetmaker´s, boot-making or tailor´s. The butcher´s guild, ratified by the king Sigismund III in 1595, was one of the most important guilds in Spisske Podhradie. This craft-agricultural town was approved to have weekly market every Thursday.
In 1412, thanks to king Sigismund of Luxemburg the town of Spisske Podhradie alongside with another 15 Spis towns was in the Polish deposit for 360 years. The deposit finished in 1772 when the sovereign Maria Theresia bought these towns from the Polish sovereign. In 1876 after the return from the Polish deposit, Spisske Podhradie became the member of Province of 16 Spis towns.
Protestants, numerical community with parish and school, had an important role among the inhabitants of the town. In 1614 there was an important synoda for Protestants in Spisske Podhradie that tossed for separation and hierarchy in an evangelic church in eastern Slovakia.
Jews, another important community, established Jewish Register Office, school and a synagogue in 1875. They were an important part of the town´s history because they strengthened business of the town.
Catholics were the largest group of inhabitants thanks to the Spis Chapter House that was the centre of the Spis area and one of the most religious European centres. It was the centre of scholarship, education and traditions of ecclesiastic singing. Since 1198 the Spis Chapter House was a priory and in 1776 it became a bishopric until the present. There is a seat of priestly seminar. Since 1993 Spisske Podhradie, the Spis Castle, the Spis Chapter House and the Church of Holy Spirit in the village of Zehra are enrolled on a list of world´s cultural and natural heritage of UNESCO.