The history of the monastery is complex and tangled, its beginnings lost in the depths of centuries. Originally, it was a girls' Holy Spirit Monastery, first mentioned in documents from 1595. In 1617, construction of a stone cathedral began here, and the work dragged on until the end of the century. In 1697, Abbess Anisya complained to Peter the Great about the prolonged construction, and he issued the necessary orders, pointing out the culprits: “To the steward and voivode Stepan Timofeevich Klokachev in Putivl. In previous years, the Holy Spirit girls' monastery and the church of God were begun to be built by our state decree and at our state treasury. The first builders of the monastery, Levoniy Lipevanov, Nikifor Yatsyn, and Ivan Dashkov, built the monastery for about ten years and more, and after them, the builders were Putivl nobles, changing annually. And these builders continued the construction for about seventy years and more. Meanwhile, now, when that monastery and the fence are being completed, there are no builders, supervisors, or a single person for the stone work.” Finally, by 1707, all work was completed, and an ensemble emerged consisting of the surviving buildings. In 1770, the monastery was abolished, and its buildings were transferred to the city’s Spassky Cathedral.

In the center of the monastery, behind a stone fence with monumental gates, rises the snow-white Spaso-Preobrazhensky Cathedral with five onion-shaped domes. This type of church is characteristic of Moscow architecture of the 17th century. The high quadrangular volume contrasts with the low porch, gallery, apses, and chapel surrounding it. Despite its monumental size, the building is elegant and corresponds to the spirit of Peter's architectural era. The walls of the main volume are adorned with narrow semi-columns, the windows are arranged in two tiers and framed with thin sculptural work. The interior of the cathedral impresses with its scale and height, generously illuminated by numerous windows, contrasting with the low darkened galleries and chapels connected to the central volume by wide arches. The walls inside are whitewashed, and the five-tiered iconostasis, rising to the vaults, looks like a fairy-tale carpet. It belongs to the type of Russian iconostases of the 17th century with horizontal cornices and vertical carved columns on a dark red background. The masters introduced local features: the royal gates have a Ukrainian opening with cut corners, and the grapevine on the columns is typical of Ukrainian baroque. In 1907, the iconostasis was restored and re-gilded under the supervision of the Imperial Archaeological Commission. No other 17th-century iconostases have survived in Left-Bank Ukraine, making the Putivl one unique.

In the center of the cathedral, a silver chandelier hangs from a long chain, made in Nuremberg and gifted by Peter the Great. It has a baroque character, emphasized by the exquisite design of the brackets. The lower sphere is decorated with an ornament reminiscent of Ukrainian jewelry from the 17th century, leading to the assumption that the chandelier's design was created by a Ukrainian master. South of the cathedral is the bell tower church of the Exaltation of the Holy Cross, built between 1697 and 1707 as the gate church of the Holy Spirit Monastery. It is two-tiered: above the western narthex rises the octagonal bell tower with a tent and dome. A two-story annex from the west, balancing the asymmetry, was erected in 1764.

The architecture of the monument is characterized by simplicity, grandeur, and power of forms. The concise architecture of the bell tower church contrasts with the sophistication of the cathedral. The cathedral is static, while the gate church is dynamic: the architectural masses rise from the apse through the central volume to the octagon of the bell tower. The latter, in addition to its cult functions, had a defensive significance, as evidenced by the loopholes at the base. An interesting page of Putivl's history is associated with this building. According to legend, after the second streltsy uprising, Peter the Great exiled Princess Sophia to Putivl, imprisoning her in the monastery. She was settled on the first floor of the gate church in a cell to the right of the gates. By Peter's order, she was kept “under strong guard,” but this seemed insufficient, and clocks were made in Holland that struck loudly every minute. They were installed under the windows of Sophia's cell so that she would not forget her “dear brother.” However, soon Peter realized that keeping Sophia in Putivl was unsafe, as she could become a “banner” for the streltsy regiments prone to uprisings. Therefore, the princess was removed, and the clocks ended up in the Molchansky Monastery in the 19th century, where their striking annoyed everyone until they were broken.