The first major Rochester station was built in 1845 by the New York Central Railroad on Mill Street by High Falls.

The station, often referred to as Bragdon Station, was four stories with three high arching windows reminiscent of train driving wheels and a main room that was reminiscent of New York's Grand Central Terminal complete with arched ceilings and a lunch counter.

In a move that is largely considered today to have been a mistake, the famed 1914 station was mostly demolished in 1965 after its sale to private owners except for the then run down western-most (one-third) portion which served as the station (with the ticket sales at the entrance to the passenger tunnel).

The passenger, baggage tunnels and one of the platform canopies of the original 1914 building were the last remaining remnants of the previous 1914 station to survive.

It opened on October 6, 2017, in a ceremony attended by Congresswoman Louise Slaughter, Mayor Lovely Warren and Governor Andrew Cuomo.

[7][8] Its construction occurred around the same time of two other Empire Corridor stations: Niagara Falls (2016) and Schenectady (2018).

On March 17, 2018, a day after Slaughter's death, Senators Chuck Schumer and Kirsten Gillibrand along with former Mayor and Lieutenant Governor Bob Duffy requested that Amtrak rename the station for Slaughter, who played a significant part in securing the funding for the rebuilt station.

The platform is connected to the station building via a tunnel underneath the tracks that is accessed by stairs, escalator and elevator.

In 2010 U.S. Border Patrol agents boarded the trains at Rochester station and asked passengers for details of their citizenship.