The church in Kopnino existed as early as the mid-16th century. A hundred record from 1563 mentions: "In the village, there is the church of Nicholas the Wonderworker." The land books of 1593 also indicate a church with the same name, but it had not yet been consecrated. It was likely a new building, served by priest Vazhen, as well as a prosphora baker and the poor who received assistance from the church. The church lands included 10 quarters of arable land and 100 bundles of hay. After 35 years, the population of the Kopninskaya estate significantly decreased, possibly due to Lithuanian devastation. According to the land books of 1628-1629, there was a monastery courtyard in the village of Kopnino, 7 courtyards for monastery arable land, and 2 courtyards of landless peasants. In the village of Svechina, there were 14 courtyards of monastery fishermen, and in the village of Zheltikovo, 5 peasant courtyards. In the village of Merinovo, there were 2 peasant courtyards, 2 landless, and 1 empty, while the village of Izmailovo was listed as a wasteland. In the census books of 1678, Kopnino is recorded as a hamlet of the village of Khupani, and the entire Kopninskaya estate was recorded together with Khupanskaya. All the mentioned villages, including the newly settled Izmailovo, had 169 peasant and 10 landless courtyards with a population of 604 men. In the 18th century, the peasants of the village of Kopnino and the surrounding villages performed duties for the Trinity-Sergius Monastery along with the peasants of the village of Khupani. From 1764, they became state peasants.

In the land books of 1628-1629, the church in Kopnino is mentioned: "In the village, there is a wooden church of Nicholas the Wonderworker, and in the church, there are a Deesis, royal doors, local icons, vestments, books, and all church property belonging to the monastery. The priest Andrew serves at the church, along with deacon Fedka and sexton Yakimko. The church land is 2 quarters in the field, 8 quarters overgrown with forest, and 100 bundles of hay." Inscriptions on the books stored in the church testify that the church in the name of Nicholas the Wonderworker existed in Kopnino in 1684.

In 1711, there were 62 parish courtyards at the church, and in 1746, a tribute of 3 rubles and 28 kopecks was collected from it. In 1775, the church burned down, but in the same year, with the blessing of Bishop Antoniy of Pereslavl, a new wooden church in the name of Nicholas the Wonderworker was built. Gavriil Ivanovich Tsvetkov, who graduated from the theological department of the Vladimir Theological Seminary in 1804, was appointed priest of the village of Kopnino in the Pereslavl district and died in 1837.

In 1815, instead of the wooden church, the parishioners erected a stone temple with a bell tower, which still exists today. It has three altars: in the cold temple of St. Nicholas the Wonderworker, and in the warm chapels, of St. Sergius of Radonezh and the Kazan Icon of the Mother of God. The church was well supplied with utensils, vestments, holy icons, and liturgical books. The altar of the main church was decorated with gilded copper boards with embossed sacred images. Among the icons, the Smolensk Icon of the Mother of God, the Icon of the Mother of God "Joy of All Who Sorrow," and St. Nicholas the Wonderworker were especially venerated by the parishioners.