Until 1950 the Far Rockaway Branch of the Long Island Rail Road was part of a loop that traveled along the existing route.

[9][10] The station also served as the terminus of a Long Island Electric Railway trolley line leading to Jamaica, via New York Avenue (now Guy R. Brewer Boulevard).

On June 11, 1952, the city acquired all trackage west of Mott Avenue, incorporating it as part of the IND Rockaway Line.

[17] Service provided by the A train over the line began in June 1956, with the full western spur to Rockaway Park operational.

[16] While the remainder of the line operated, with Beach 25th Street–Wavecrest serving as the eastern spur terminal,[16] a new Far Rockaway subway station was constructed, opening on January 16, 1958.

[6][15][22][23] The original site of the LIRR's elevated station and the bus depot, located on the northeast side of Mott Avenue, were replaced with a shopping center and parking lot,[6][22][23][24] which began construction in 1960.

At Far Rockaway, the 1950s design of the station house was replaced with metallic facades and a dome enclosure, and upgrading several features including staircases and employee areas.

The Far Rockaway–Mott Avenue station, the Rockaway Line's eastern terminus, is built on a concrete viaduct and has two tracks and an island platform.

[5] Under normal service patterns, it is served by the A train at all times[42] and is its southern terminus; the next stop to the west (railroad north) is Beach 25th Street.

[44][45] The doors at the northeast end of the platform lead to stairs down to the street level fare control area.