Vepriai was founded on a hill near Vepriai Lake and south of Šventoji River.
It is first mentioned in Wigand of Marburg's Chronicle of 1384 under the name of Weperen.

In the Middle Ages Vepriai was a powerful hill fort which assisted in protection of Lithuanian lands from western threats, primarily the Teutonic Order.
Wigand of Marburg asserted that the castle belonged to the Grand Duke of Lithuania.
In spring of 1384, during the Lithuanian civil war of 1381–1384 the united forces of Grand Duke of Lithuania Vytautas, under command of Nartautas, and the Teutonic Order, attacked the castle which was under control of Jogaila or Skirgaila and captured it.
After the threats were eliminated, in the place of the destroyed wooden defensive castle on a piliakalnis a residential manor was built, ruled by various noble families for several centuries.

At the time of the first mention in 1542, the castle's owners were the Kęsgailos Lithuanian ducal family.
At the turn of the 17th century the Renaissance residential palace of the Šemetos noble family was built.
Then it passed to the Ogiński ducal family.
The place owned by Alexander Ogiński (1590–1653) became a dowry of his daughter Barbara Szemiott née Ogińska in the 17th century and thus passed to the Szemiott (Šemetos) family but was taken back by Barbara's nephew Marcjan Aleksander Ogiński in 1681.
Later it passed to the Tyzenhauz family (again as a dowry) and eventually became disputed between it and the Kossakowski family until 1779.
In 1808 Count Ignacy Tyzenhauz sold it to Count Jozef Dominik Kossakowski.
Following his death in 1840 the place was inherited by Kossakowski's daughter Pelagia, married to a Scottish esquire, former servant in the Indian Navy, Alexander Bower St. Clair, father of an infamous rebel leader Stanislas Saint Clair, born in the manor palace.
In 1855 the place once again changed hands, as it was sold to Ksawery Podbereski and his wife Anna née Roemer, who later sold it to Count Adam Alfred Plater.
The Plater family owned the palace and the surrounding lands until 1923, when the area was nationalized by the Lithuanian state.

The 17th century Renaissance palace on the Vepriai Mound was devastated by Swedish troops during the Great Northern War and has been demolished later on.
The other place closer to the lake has been selected for the new palace.
The present Neoclassical palace was erected in the 19th century and is dominant in the manor ensemble.
Countess Emilia Plater with her army has stayed in the manor during the November Uprising.
The manor was nationalized in 1923 and has been used to house the newly established Vepriai Agricultural School since 1924.

Vepriai became the center of the new parish in 1845 and was the capital of Vepriai Volost from 1864 until 1950.
Vepriai was founded on a hill near Vepriai Lake and south of Šventoji River. It is first mentioned in Wigand of Marburg's Chronicle of 1384 under the name of Weperen.
In the Middle Ages Vepriai was a powerful hill fort which assisted in protection of Lithuanian lands from western threats, primarily the Teutonic Order. Wigand of Marburg asserted that the castle belonged to the Grand Duke of Lithuania. In spring of 1384, during the Lithuanian civil war of 1381–1384 the united forces of Grand Duke of Lithuania Vytautas, under command of Nartautas, and the Teutonic Order, attacked the castle which was under control of Jogaila or Skirgaila and captured it. After the threats were eliminated, in the place of the destroyed wooden defensive castle on a piliakalnis a residential manor was built, ruled by various noble families for several centuries.
At the time of the first mention in 1542, the castle's owners were the Kęsgailos Lithuanian ducal family. At the turn of the 17th century the Renaissance residential palace of the Šemetos noble family was built. Then it passed to the Ogiński ducal family. The place owned by Alexander Ogiński (1590–1653) became a dowry of his daughter Barbara Szemiott née Ogińska in the 17th century and thus passed to the Szemiott (Šemetos) family but was taken back by Barbara's nephew Marcjan Aleksander Ogiński in 1681. Later it passed to the Tyzenhauz family (again as a dowry) and eventually became disputed between it and the Kossakowski family until 1779. In 1808 Count Ignacy Tyzenhauz sold it to Count Jozef Dominik Kossakowski. Following his death in 1840 the place was inherited by Kossakowski's daughter Pelagia, married to a Scottish esquire, former servant in the Indian Navy, Alexander Bower St. Clair, father of an infamous rebel leader Stanislas Saint Clair, born in the manor palace. In 1855 the place once again changed hands, as it was sold to Ksawery Podbereski and his wife Anna née Roemer, who later sold it to Count Adam Alfred Plater. The Plater family owned the palace and the surrounding lands until 1923, when the area was nationalized by the Lithuanian state.
The 17th century Renaissance palace on the Vepriai Mound was devastated by Swedish troops during the Great Northern War and has been demolished later on. The other place closer to the lake has been selected for the new palace. The present Neoclassical palace was erected in the 19th century and is dominant in the manor ensemble. Countess Emilia Plater with her army has stayed in the manor during the November Uprising. The manor was nationalized in 1923 and has been used to house the newly established Vepriai Agricultural School since 1924.
Vepriai became the center of the new parish in 1845 and was the capital of Vepriai Volost from 1864 until 1950.
Vepriai