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Telšiai parish was founded in 1536, the same year when the Duke of the Grand Duchy of Lithuania Sigismund the Elder ordered the construction of the Church of the Holy Assumption of Virgin Mary. Later, in 1612, the church started housing the newly established Telšiai parish school. However, the church could not survive the test of time.
In 1700, the first church was replaced with a new wooden church. Unfortunately, with the Great Northern war starting in the same year, the church was devastated almost immediately. In 1788, after a long period of armed conflict, plague, and famine, a reconstruction of the church finally started. However, not all was well, as couple of decades later, in 1814, the Russian Tsarist government closed and soon demolished the church. After the Novermber Uprising of 1831, the Tsarist government doubled-down on its anti-Catholic policy by confiscating the lands of the church and destroying the cemetery on Vilnius hill.
In 1867, the demolished church was replaced by a neo-Byzantine style Church of St. Nicholas the Wonderworker. The church was much more luxurious than the previous ones, boasting a 50 meter tower, flashy interior containing many icons and luxurious, decorated liturgical books. This sort of extravagance was employed all over the Catholic areas of the Russian empire as a futile attempt to convert catholics to Eastern Orthodoxy.
The Telšiai parish regained the ownership right to their land only in 1935 and a new catholic church was built. During the Soviet occupation of Lithuania, the Soviet government made several attemtps to close down the church, but it was prevented by a strong opposition from the community.
Although the Church of the Holy Assumption of Virgin Mary was renewed again in the 21st century, it still retains features of a wide variety of architectural styles, including neo-Gothic, Neo-Baroque and Neo-Byzantine influences.