[4][5][6][7] Avenue X station opened as the line was extended from Kings Highway at noon on May 10, 1919.

[15][16] BMT Culver Line (5) trains were truncated to Ditmas Avenue, the south end of the connection, operating through to Manhattan via the Nassau Street Loop during the day, and terminating at Ninth Avenue at other times.

[19][20][21] The station was renovated from June 29, 2015 to December 28, 2015 (Manhattan-bound platform) and June 7, 2016 to May 8, 2017 (Coney Island-bound platform with trains bypassing on the center track) as part of a $140 million renewal project on the Culver Line.

[22][23][24][25] In May 2018, site specific permanent public artwork created by NYC based American artist Derek Lerner was installed at this station.

[28] The southbound side has an exit-only staircase at platform level[28] that was used primarily to direct customers to the F shuttle bus to Coney Island–Stillwell Avenue when it was closed for reconstruction from September 2002 to May 2004, and this station was used as a terminal.