The church was built in the first quarter of the 14th century in an elevated position. The permission to build the church dedicated to St. John the Evangelist on the property of Peter and Tomáš, sons of Master Filip Donč of Zvolen, was issued by Archbishop Tomáš of Esztergom in 1310. By the end of the first quarter of the century it seems to have stood.

It was a typical village church of those times. The simple building consisted of a longitudinal nave, a square presbytery and a northern sacristy. Similar buildings can also be found in nearby Čerín or Horná Mičina.

Already in 1325, the Franciscan chapter from the monastery in the nearby Slovenská Ľupča was held in the church and the Franciscan motifs are reflected in the fresco decoration, which dates back to two main stages (around 1380 and 1415). However, it is not clear when the patronage was changed to the present one.

In the last third of the 15th century, modifications in the late Gothic style were carried out in several stages. Around 1470, the south window of the presbytery was enlarged and several architectural elements and lining were painted red (renewed in the last restoration in the 20th century). A large painting of the Ladislaus Legend on the north wall of the nave dates from 1478.

A significant intervention in the form of the church was the late Gothic reconstruction dating back to the period around 1490 (the literature also mentions the year 1512 and 1478). It included the addition of a side chapel opening into the nave with a semicircular arch on the north side (an unknown image under the painting of St George and a large part of the Nativity of St John the Baptist were destroyed) and a smaller ossuary, the western wall of which is at the level of the west front of the church. The newly added chapel was at the same time decorated with murals. The west portal in this façade was also created at this time.

At the beginning of the 16th century, minor alterations were made to the interior, but also the paintings in the interior and exterior were painted over. During the Reformation, the church was used alternately by Protestants and Catholics. The church and the whole village fell on hard times in the second half of the 17th century, when Poniky was twice sacked and burnt down by Turkish troops (1663 and 1678). During this period, the church was even used as a stable for the Turks. In 1709 the church finally belonged to the Catholics. The construction of the fortification of the church dates back to the 16th century.

The extensive Baroque reconstruction was carried out between 1752 and 1764. The church received new interior furnishings and the nave and chapel were vaulted with brick. In the western part of the nave a brick tribune was built. The Gothic windows of the nave and the south portal were also bricked up. The nave was newly lit by two larger windows. The lighting of the north chapel was also redesigned, where instead of the two original bricked-up windows, one new one was broken through, located in the middle of the north wall. A new window was also created in the north wall of the sacristy. In 1778 the brick tribune was enlarged with a wooden imaginary part.

In 1810, a brick foundation of the belfry was added to the western front, which was followed by a wooden superstructure. In the lower part of the bell tower a so-called begging room was built.

Minor modifications were also carried out in the following decades of the 19th and 20th centuries. The turning point in the history of the church came in the second half of the 20th century. In 1961, parts of the wall paintings in the attic space were uncovered; ten years later, restoration research began, followed by a comprehensive restoration that included solving structural problems (including the removal of the Baroque vault and bell tower), reconstructing bricked-up architectural details, and restoring the wall paintings. The work was completed in 1992.