The Prospect Avenue station was constructed as part of the Fourth Avenue Line, which was approved in 1905. Construction on the segment of the line that includes Prospect Avenue started on December 20, 1909, and was completed in May 1912. The station opened on June 22, 1915, as part of the initial portion of the BMT Fourth Avenue Line to 59th Street. The station's platforms were lengthened in 1926–1927, and again during a renovation in 1968–1970. The station was also renovated in 1970 and 2017.