The first mention of the church at the Pukhlimo burial site is found in the Kashin inventory book of 1628-1629: "The burial site of Nicholas on the Pukhlenka River, and in it a church in the name of Nicholas the Wonderworker, and the chapel of the great martyr Paraskeva, a wooden chapel."

Over time, the wooden church fell into disrepair, and in 1716, a new wooden Nicholas church was built in its place. By the end of the 18th century, it became too small for the growing number of parishioners and was in poor condition.

Prince Pyotr Nikolaevich Volkonsky, a local landowner and parishioner serving in Moscow, decided to build a new stone church at his own expense. In 1790, he submitted a request to the Tver archbishop Tikhon for permission to construct the church, asking to build it not at the previous site but in his estate in the village of Otrubnevo.

The construction was delayed for many years for various reasons. In 1805, the side chapels with altars in honor of the martyr Paraskeva and saints Peter and Paul were completed. Presumably, the bell tower was built around the same time. In November 1805, Archimandrite Nikifor of the Novotorzhsky Borisoglebsky Monastery consecrated them, and services began in the chapels. The old wooden church at the Pukhlimo burial site was dismantled.

In the early 1900s, the refectory with chapels was expanded. The work was overseen by provincial architect V. I. Nazarin. During the reconstruction, the project was slightly altered, and the refectory was expanded only between the cold church and the bell tower. The updated chapels with altars of saints Peter and Paul and the martyr Paraskeva were consecrated in 1906. Now the church could accommodate up to 735 parishioners.

In 1962, the church was closed. In 1963, according to a resolution of the Kalinin regional executive committee, the church buildings were transferred to the local collective farm, and a grain storage facility was placed in the church building.