This station opened on July 2, 1878 when the Brooklyn, Flatbush and Coney Island Railway established it as the Brighton Line's temporary northern terminus on what was then known as the Willink Entrance to Prospect Park.

On August 18, 1878, the line was completed north to Bedford Terminal with a connection to the Long Island Rail Road.

In 1918, the station began a rebuilding in order to accommodate the new subway connection to the Manhattan Bridge and Montague Street Tunnel.

This rebuilding contributed to the Malbone Street wreck on November 1 of that year, when a train of elevated cars derailed on the then-new curve leading to what is now the unused southbound outer track.

[3][4][5] On August 1, 1920, a tunnel under Flatbush Avenue opened, connecting the Brighton Line to the Broadway subway in Manhattan.

Some of the funds would be used to renovate nearly one hundred New York City Subway stations,[9][10] including Prospect Park.

[15] In November 2019, officials installed a bronze memorial plaque at the Prospect Park station's northern exit in commemoration of the Malbone Street Wreck.

At the south end of the station, there are crossovers and switches as the Brighton Line becomes a four-track corridor to Ocean Parkway.

[21] There is a bank of turnstiles, a waiting area that allows a free transfer between directions and a token booth inside the station house.

[23] An inscribed bronze plaque to the Malbone Street Wreck, installed in 2019,[16] is located on the wall outside the northern exit.