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It is believed that the church burned down in 1394, when Lithuanians set fire to Merkinė Castle, withdrawing the army for the defence of Vilnius. Or it may have been burned down by the Crusaders in 1403. A Dominican monastery was established in 1607, and a brick church was built in 1615.


In 1676, a Jesuit monastery and a church were built here. The church was damaged in 1655, but repaired until 1674. In 1744, the parish of Merkinė had 66 villages on both sides of the river Nemunas. In 1725–1773, there was an active minor Jesuit College; in 1774, it became the property of the Dominicans who established a school here in 1776 which was used as a district school until 1831.


The parsonage and all three of its Catholic churches: parish, Dominican and Jesuit burned down during a town fire on 16 July 1822. The church of the Dominican monastery which was closed down after the uprising of 1831 was transferred to the parish. The building of the monastery was used as police and border guard headquarters. In 1843, priest Kajetonas Aleknavičius built a parsonage from his own funds. In 1884, a vestibule was built according to the project of M. Strebeika.


In 1912, the interior of the church was decorated, a parsonage was built and Polish services were no longer held under the care of Kazimieras Ribikauskas who was the pastor of Merkinė in 1911–1934. Later on, vicar M. Cijūnaitis formed an excellent Lithuanian choir together with the organist Sčesnulevičius. In 1912–1914, there was an active Division of Lithuanian Catholic Temperance Society which was allowed to establish a library - reading room in 1913. During the same year, a division of Society Rytas was established. After World War I, composer Teodoras Brazys and Dr. Juozas Bakšys worked in Merkinė. They were exiled from Vilnius for their Lithuanian activities by the governor of Vilnius diocese prelate K. Michalkevičius. T. Brazys collected Lithuanian songs in the surrounding areas of Merkinė, while priest Dr. J. Bakšys established a progymnasium in 1921 and was its director. On 17 December 1924, he was injured with two shots fired by malefactors, and died on 7 January 1925.


After World War II, the pastors of Merkinė were Zigmas Komaras, a Siberian exile, as well as dean Andrius Juknevičius who was killed by Bolsheviks in Kaišiadorys. Petras Laskauskas (1903–1988) was the pastor since 1966 and was buried in the churchyard after his death.


The church itself is of the Gothic period with Baroque features added after the reconstruction. It is a two-tower church with a three-sided apse. The interior has three naves separated by columns. The presbytery is separated from the naves with three arches of triumph. The fence of the churchyard is masonry. The churchyard includes the cemetery of local priests.


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