In 1900, the construction of a church began in the estate of the Princes Tenishev in Talashkino, in the village of Flenovo near Smolensk. By 1905, the work was nearly completed. There are still debates about who exactly developed the architectural project of the church. The most common opinion is that Princess Maria Klavdievna Tenisheva worked on the project together with archaeologist I.F. Barshevsky and artist S.V. Malyutin. The interior of the church was painted by Russian philosopher and artist Nikolai Roerich, who also created one of his greatest works here, the mosaic "The Savior Not Made by Hands," depicting the face of Jesus. This expressive mosaic adorns the facade above the entrance to the church, drawing attention with the blue eyes of the Savior.

Prince Vyacheslav Tenishev, Maria Tenisheva's husband, was against the construction of the church. However, after Tenisheva appealed to the Smolensk governor Vasily Sosnovsky, who was a friend of the prince, V.N. Tenishev allocated funds for the construction. Tenisheva wrote that she had long sought a suitable place for the church and finally found it on a beautiful hill surrounded by pines, firs, and linden trees, with a magnificent view. Here, next to the school, the foundation of the church in the name of the Holy Spirit was laid.

Despite its small size, the church looks monumental and is an example of the neo-Russian style of the early 20th century. At this time, the focus shifted from the exact copying of ancient Russian architecture to the emotional traditions of Russian culture. The facades are decorated with ceramic tiles and mosaics, while the windows feature stained glass.

The architecture of the church differs from traditional Russian church architecture. It combines images of Russian antiquity, silhouettes of the local nature, and elements of various cult structures. The building resembles a pyramid, a Russian tent, and a Buddhist pagoda. The interior space of the Church of the Holy Spirit is arranged so that the altar is almost completely open for viewing. According to art historian Lyudmila Korotkina, the church was meant to symbolize the complexity and unity of the world. The interior paintings convey the eternity of spiritual values and assert that the meaning of life lies in filling the world with goodness. The altar composition "Queen of Heaven" embodies not the canon of one religion but is a composite image of goodness and creation in different faiths. The church is dedicated not to the Descent of the Holy Spirit but to the Holy Spirit itself, which is why it was not consecrated by the Orthodox Church. Art historians note its influence from folk religious traditions, Russian wooden architecture, Eastern teachings, and Catholic iconography.

Over time, the building of the church began to deteriorate. In April 2016, after the appeal of the governor of the Smolensk region to Deputy Prime Minister Olga Golodets, the Ministry of Culture of the Russian Federation allocated more than 40 million rubles for its restoration. A year later, more than 6 million was directed towards updating the mosaic. The Church of the Holy Spirit restored the brickwork, pavement, and basement areas, which occupy about 60% of the building's area. The restorers preserved the remaining paintings and plan to restore them based on photographs taken by Tenisheva and Roerich, as well as on the original sketches of the artist stored in the Library of Congress in the USA. An exhibition dedicated to its history is planned to be opened in the church.

The Church of the Holy Spirit in Talashkino is a cultural heritage site of the peoples of Russia. Today, it attracts pilgrims and tourists from various countries.