Dieveniškės has been mentioned since the end of XIV century. In the second XV a. In the second half of the XV century, Dieveniškės became a town and was first mentioned as a town in 1582. In 1542 after the death of Stanislovas Goštautas, it was passed to the Grand Duke and became the center of the eldership. In the acts of 1561-1565 Dieveniškės were called the royal county.

After the fire that happened in 1783 the city center was reconstructed, the current wooden church was built. From the XVII century the right to hold bazaars and three fairs twice a week, wasgranted. The privilege states that "Trade brings prosperity to cities and towns". In 1802-1950 became a county center. In 1851 Dieveniškės had a fire, in 1912 it burned.

In 1903 a brick belfry was built. Dieveniškės suffered severely during the First World War. In 1920-1939 the town was occupied by the Polish, so the Polish language became official, the Polish ethnographic self-awareness was introduced forcibly. Although Polish law provided the right for national minorities to education in their mother tongue, but since 1925 schools that were educating in other than Polish language were started to get closed.

It is said that in 1939, in Kremlin, Stalin‘s pipe was lying on the map while drawing the borders of the Vilnius region that was returned to Lithuania. No one has dared to move it, and therefore defined the line of the state border.