After the 1917 revolution, many Russian emigrants settled in France, including in Lyon. In 1924, General Pavel Maximovich-Vasilkovsky arrived in Lyon and established an Orthodox church in his apartment in honor of the Protection of the Holy Virgin, where Priest Andrei Mishin began to serve. Soon, a community formed in the city, which rented a hall in the center and set up a portable iconostasis there.

In 1926, after the schism of the Russian Orthodox emigration in Western Europe, the Protection Church remained under the administration of Metropolitan Evlogy (Georgievsky). However, part of the Russians in Lyon preferred to remain under the jurisdiction of the Archierarchical Synod chaired by Metropolitan Antoniy (Khrapovitsky). They planned to build a stone church in memory of Russian soldiers, but funds were insufficient. Eventually, they found a wooden barrack on Baraban Street, and on May 11, 1928, a new church dedicated to St. Nicholas the Wonderworker was founded. Priest Viktor Pushkin was sent to Lyon, and the iconostasis was painted by parishioner Lyudmila Galich.

With the rise to power of the Popular Front in France in 1936, Russian emigrants faced difficulties. Organizations were dissolved, and assistance was provided to Soviet counterintelligence. Protopresbyter Viktor Pushkin received threats, and on the night of June 13, 1937, the church burned down. Despite the challenges, it was decided to build a stone church. After long searches, construction of a new church for 200 people began on May 7, 1938. Protopresbyter Viktor became the inspiration for the project, and the architect was Sergey Bazderev. Frenchman Jules Roche lent 50,000 francs. The church was built by hand, despite the war and economic hardships.

On August 31, 1945, the parish came under the jurisdiction of the Moscow Patriarchate, and on May 5, 1946, the church was consecrated. In 1948, the parish returned to the jurisdiction of the Russian Orthodox Church Outside Russia (ROCOR). After the war, due to financial difficulties, the finishing of the church progressed slowly. From 1950 to 1953, Archimandrite Antoniy (Bartoshovich) served in the church, who painted the iconostasis. In the 1970s, the ceiling collapsed, and repairs required significant expenses.

In 1978 and 1980, a new church house was built, and in 1981, the church was faced and the dome painted. In 2000, the parish's active members opposed reconciliation with the Church in the Homeland and in 2001 joined the non-canonical ROCOR (V). In 2002, part of the parishioners returned to the canonical ROCOR, founding a home church of Martyr John of Russian.

In 2006, the parish came under the omophor of the Russian True Orthodox Church. In 2010, together with Bishop Iriney (Klipenstein), the parish moved to the non-canonical jurisdiction of ROCOR under the omophor of Agafangel (Pashkovsky). In 2012, Iriney reported on the good condition of the parish, regular services, and the presence of candidates for the priesthood.