Since 1836, a new Guard Corps of the Life Guards was stationed in Oranienbaum. At that time, there were only two churches in the city, and they were far apart, so there was not enough space for everyone. With the arrival of the military, the field church of Spyridon of Trimythous was temporarily placed in a private merchant's house.

Two years later, on October 2 (14), 1838, the construction of a wooden church of Spyridon of Trimythous began in the upper part of Lomonosov, at the beginning of Ilikovsky Avenue, near the palace park. The church was built with state funds according to the design of architect Melnikov, who adhered to strict classical forms and preferred the Empire style, popular in Russia after the 1812 war.

The church was built quickly but solidly: the building in the shape of a ship was erected on a brick foundation, measuring more than 10 meters in width and about 26 in length. The roof, at a height of eight and a half meters, was covered with iron, and the interior was adorned with a field iconostasis featuring an icon of Saint Spyridon. On the day of his memory, December 12 (25), 1838, the new church was consecrated.

Later, the church was expanded by adding two side chapels without altars to increase space. The interior was updated with a three-tiered white iconostasis with gold. Now the building could accommodate more parishioners and matched its status.

To attract townspeople and create a festive atmosphere, singers were invited to the services. In the summer, the choir included students from the Women's Patriotic School, which was sponsored by Grand Duchess Ekaterina Mikhailovna.

The church's income was insufficient to maintain order, and the building fell into disrepair. Parishioners preferred to visit the Church of Archangel Michael. It took a lot of effort to update the sacristy, establish heating, and hold regular services. This paid off, and nine thousand rubles were raised for the construction of a new church.

In the fall of 1895, the old building was dismantled, and a new foundation was laid. The project for the new church was created by Captain V. I. Shcheglov, who also oversaw the construction. A year later, the work was completed, and on September 8, 1896, the new church of Spyridon of Trimythous was consecrated. Representatives of the military and church leadership were present at the ceremony, and the choir of Kazan Cathedral performed hymns.

The new church became the spiritual center of the city, housing church and military relics, and later a library. In the late 19th century, the church was visited by John of Kronstadt.

In the early 20th century, the fate of the church turned tragic. During World War I, the church served as a spiritual support for the military and their families. With the onset of the revolution and anti-religious reforms, the church lost its independence and was attached to other churches. In 1930, it was closed and desecrated. The building was used as a warehouse, then as a Pioneer House and gym. The city was renamed Lomonosov.

In the early 2000s, the church was returned to the faithful, but the building was in emergency condition. In 2001, it was included in the list of cultural heritage sites, but its condition remained dangerous. In 2008, reconstruction began.

The restoration required a lot of effort and funds. In 2008, the wooden church was dismantled, and over five years, a frame and walls, domes, and roofing were erected. The old foundation and additional supports were used. By 2012, eight new bells were cast and a fence was installed.

In 2013, finishing and communication works began. A cross was erected over the dome, and the iconostasis and interior space were arranged. By 2016, the church was restored to its original form from 1896.

In August 2016, 120 years after the construction of the second church, services resumed. Inside the church, a harmonious space was created with a wide dome and side chapels, illuminated by bronze chandeliers and heated by stoves. The choir is located at the entrance, and under the bell tower, there is a room for the sacristy and library.

The walls and ceilings were painted pale pink and decorated with carvings. The iconostasis features icons of the Savior, the Mother of God, and saints. The main relics include icons of Saint Spyridon and Saint Nicholas.

The interior of the church is designed in light tones and decorated with carvings, creating a cohesive space. The altar is adorned with a chandelier featuring intricate ornamentation. The tier of stained glass windows fits organically into the atmosphere of the church.

The modern iconostasis, like in 1896, is white. Temple icons are placed in the kiots around the perimeter. The only contrasting element to the overall spirit is the image of the Cross of the Lord, reminding of the transience of life.

The decoration of the church reflects the harmony between the earthly and the heavenly, symbolizing purity and rebirth.