Most of the 1915-built station is occupied by the 1972-opened Brattleboro Museum and Art Center, while Amtrak uses a waiting room on the lower floor.

[2] The Brattleboro and Whitehall Railroad, a CV subsidiary, opened to South Londonberry, Vermont in 1880.

[3]: 173  The B&M opened the Fort Hill Branch of its subsidiary Ashuelot Railroad between Brattleboro and South Vernon in 1913; it was operated as a second track of the existing CV mainline.

[3]: 58  In 1972, the town purchased the disused Union Station building for $27,500 (equivalent to $152,000 in 2023); it was converted to the Brattleboro Museum and Art Center, which opened that year.

[4] Amtrak, which took over intercity passenger rail service in the United States in 1971, began operation of the overnight Montrealer on September 30, 1972.

Brattleboro was a stop for the Montrealer from its inception, though a ticket office and waiting room did not open in the lower level of the Union Station building until 1973.

[5][6][7][4][8] A $366,000 expansion of the parking area, which involved demolition of the nearby Archery Building, was completed in 2021 ahead of the station project.

[12] In October 2021, the town proposed to transfer ownership of the station building to the museum for $1, contingent on Amtrak vacating its portion by mid-2024.