Built by the Anglo-Newfoundland Telegraph Company, between 1870 and 1880, the Avondale Railway Station served as a repeater station for the first telegraph land line serving St. John’s. From 1900 to 1949 the structure was a freight and passenger station operated by the Reid Newfoundland Company, and was an important terminus during World War II for transporting men working at the American Military bases in Argentia.

Now the oldest surviving railway station in Newfoundland, from Confederation in 1949 until its closure in 1984, the Canadian National Railway (CN) used the station as a terminus for their passenger and freight service in Conception Bay, until its closure in 1984. In 1985 the Town of Avondale acquired the Railway Station from CN Railway.

The Avondale Railway Station was designated a Registered Heritage Structure by the Heritage Foundation of Newfoundland and Labrador in 1988.