The station was originally built sometime in the summer of 1882. However, Bellport's station house was closed in January 1959 and razed in May 1964, but not before being replaced with a sheltered-shed. A depot with a high-level platform were built between 2000 and 2001, which many stations on the LIRR were getting at the time. Bellport Station serves as the replacement for Brookhaven Station, which was closed by the LIRR on October 6, 1958.
This station has one high-level side platform on the south side of the tracks that is long enough for one and a half cars to receive and discharge passengers. The Montauk Branch has two tracks at this location. The north track, not adjacent to the platform, is a siding.
Another Bellport Station existed along the Main Line sometime in 1844 with the opening of the LIRR. Located 2½ miles (4 km) east of Medford Station and thus much further north than Bellport, it included a stagecoach connection to Bellport Village, hence the station's name. This would eventually be renamed Bartlett Station, and was abandoned at some point.