The original Cortlandt Street station was built by the Interborough Rapid Transit Company (IRT) and opened in 1918 as part of the Dual Contracts.

Around that time, the portion of Cortlandt Street above the station was demolished to make way for the World Trade Center.

[8] It was predicted that the subway extension would lead to the growth of the Lower West Side, and to neighborhoods such as Chelsea and Greenwich Village.

[9][10] Cortlandt Street opened as part of an extension of the line from 34th Street–Penn Station to South Ferry on July 1, 1918.

[11][13] The new "H" system was implemented on August 1, 1918, joining the two halves of the Broadway–Seventh Avenue Line and sending all West Side trains south from Times Square.

[14] An immediate result of the switch was the need to transfer using the 42nd Street Shuttle in order to retrace the original layout.

[16] There were mosaic decorations by Squire J. Vickers or Herbert Dole depicting ships along each platform's wall.

[29]: 8C-3 The station and the surrounding subway tunnels were severely damaged in the September 11, 2001, terrorist attacks following the collapse of Two World Trade Center, resulting in the closure of the line south of Chambers Street.

[32] Soon after the attacks, two options were considered: either the existing line would be repaired, or the tunnel would be diverted westward just to the north of the World Trade Center site before heading to a new terminal at South Ferry.

[35] As part of the project, the East Bathtub was extended under the line to the eastern boundary of the site at Church Street.

"[36] The Port Authority's chief engineer and others tried to convince him to temporarily shut down the line while the new transportation hub at the World Trade Center was under construction.

The Governor's decision to keep the line open increased the cost of the project because the subway structure had to be underpinned.

[41] In 2007, the Port Authority of New York and New Jersey (PANYNJ), in the Environmental Impact Statement for the World Trade Center PATH terminal, expected the Cortlandt Street station to reopen in 2009.

[29]: 8C-16  In October 2008, the PANYNJ stated in a report that it had come to an agreement with the MTA on reconstructing the Cortlandt Street station.

[25] Disputes between the PANYNJ and the MTA over who would pay for the renovation had caused the planned opening of the station to be delayed from 2014 to 2018.

[51] The renovation included new Americans with Disabilities Act-compliant entrances with elevators,[51] track-intrusion systems, fire alarms, Help Points, CCTV cameras, countdown clocks and air conditioning.

[48] By September 2017, much of the communications, power, and ventilation infrastructure was being installed, but contractor work and Port Authority utility relocation were significantly delayed.

According to the MTA's Capital Program Oversight Committee, the contractor had to more than double its productivity to ensure an October 2018 opening, with substantial completion in December 2018.

[57] Station name signs with the text "World Trade Center" were being installed along the platform walls by August 2018.

On September 7, 2018, several news sources reported that the station would reopen the next day in time for the seventeenth anniversary of the attacks.

[69][72][44] There are columns between the tracks, except where the station passes over the World Trade Center Transportation Hub toward its north end.

The WTC Cortlandt station is located just west to the World Trade Center Hub's head house, which is known as the "Oculus".

[2] Two mezzanines underneath the tracks, at the north and south ends of the station, give direct access from the subway to the PATH.

[73] There are additional entrances to the uptown platform from the Oculus building's upper balcony, as well as from the South Concourse, which connects to the basement of 3 World Trade Center.