The oldest known Valkininkai church dates back to 1555. foundation. 1611 the inventory mentions a newly built church near the marketplace. 1635-1650 A brick monastery with a church was built in Valkininkai.
1655 the parish church burned down and was soon rebuilt. In place of 1772 a temporary one built by the burnt parish church, which in 1818 January 17 storm destroyed. The service has been moved to the graveside chapel. Since 1777 there was a parish school.
In 1822, in addition to the jurisdiction in the town, the villages of Kuklii and Puodzii belonged to the parish church. The monastery had jurisdiction in Valkininkai and the village of Curonian Spit. The Russian authorities closed the monastery in 1832. closed and turned into barracks. Monastery Church 1832-1837. used by parishioners. After 1837 the authorities transformed it into an Orthodox army church in 1883. rebuilt into a public church. 1941-1944 there was a prisoner of war camp. 1944 the Nazis blew up the building.
1822-1837 the present brick church was built. She was born in 1854. consecrated by Bishop Vaclovas Žilinskas. Back in 1881 requested permission to enlarge the parish church. The authorities did not allow it, and the pastor V. Živoronokas was removed from Valkininkai for collecting donations. 1885 a new church enlargement project was prepared. It was not allowed to build again, because the church would have overshadowed the Orthodox church in its appearance. 1895-1898 the church was enlarged.
In Valkininkai 1884-1892. Pastor Silvestras Gimžauskas (1844-1897) complained to the authorities about the distribution of the Lithuanian press, because of his undesirable influence on the government school. Several cases were filed against him. At the request of the authorities, S. Gimžauskas was removed from Valkininkai. Since 1918 Pastor Jonas Karvelis (1874-1933) was persecuted by the Polish authorities, in 1927. arrested and deported to independent Lithuania.
1944 The pastor of Valkininkai, Juozas Bardišauskas, asked the Nazis to allow them to bury the victims of the village of Pirčiupiai. Later, he headed the local underground organization "Lietuvos partizanų sąjunga". 1946-1949 Pastor Stanislaus Kakarieka was persecuted and punished for catechizing children. In 1970 and 1973, pastor Algimantas Kane was in power. prevented the repair of the church.