Construction began on December 15, 1845, and the first section, from White River Junction west to Bethel, opened on June 26, 1848.

[1] In 1867 the Vermont Central leased the Stanstead, Shefford and Chambly Railroad, running east from St. Johns to Waterloo, Quebec.

[1] Though the Missisquoi Railroad was chartered as an independent entity in 1867, the Central Vermont RR gained control of it shortly thereafter.

It was formally leased in July 1873, providing a branch from St. Albans northeast to Richford, Vermont.

The company was reorganized in December 1886 as the Missisquoi Valley Railway, and was once again leased to the Central Vermont.

The main line ran from the Grand Trunk Railway's Montreal and Champlain Railroad at Saint-Lambert, across the St. Lawrence River from Montreal, southeast to Farnham on the Stanstead, Shefford and Chambly Railroad, with an extension continuing southeast to Frelighsburg.

[1] On July 12, 1920, the entire Grand Trunk system was placed under the control of a "Board of Management" by the federal Department of Railways and Canals in Canada after several years of financial difficulties.

[1] While the Central Vermont was no longer independent, it kept much of its corporate identity and was run as a separate railroad from the rest of the CN system.

As the grip of the Great Depression eased, the railroad became a relatively successful arm of the CN network until the postwar period.

It moved a wide range of freight from general merchandise and furniture to milk and agricultural products.

[1] During the 1950s, diesels from CN began to appear on the Central Vermont, with the last steam locomotive ending service in 1957.

Under the Grand Trunk and later the Canadian National, the Central Vermont system saw many of its unprofitable branch lines abandoned.