The railway station was built approximately 20 meters from the Entrance Gateway by architect Giuseppe Momo. The station building is composed of white marble, and its dimensions are 61 by 21.5 meters.
The construction of a railway station in Vatican City and its linkage to the Italian rail lines was guaranteed by the Lateran Treaty of 11 February 1929.
The first locomotive entered the Vatican in March 1932. The station was opened officially in 1934. A Railway Convention was ratified between Italy and Vatican City on 12 September 1934, on which date the property passed from the Italian State Railways to the Holy See.