The South Side Railroad of Long Island and Central Railroad of Long Island once had another station in Copiague to the east called Belmont Junction, which was in service between 1873 and 1885.

[2] It is not known if the Long Island Rail Road built Copiague Station as a replacement for Belmont Junction, but it had served as one.

[3][4][5] Copiague Station was originally built in 1902 and was rebuilt with temporary high-level platforms for the M1s on October 25, 1968.

In 2023, the MTA agreed to make the Amityville, Copiague, and Lindenhurst stations wheelchair-accessible to settle a lawsuit.

[7][8] This project brought the station into compliance with the Americans with Disabilities Act.