The railroad, also known as the Castleton Company, received its charter from Vermont in 1848 and opened in 1850.
[1] It also operated a 1.51-mile (2.43 km) branch line from west of Castleton north along Lake Bomoseen which served local slate quarries.
[3] From March 14, 1865 the Rensselaer and Saratoga Railroad leased both companies and operated them together.
The Delaware and Hudson Company, which already controlled the Rensselaer and Saratoga, took over operation of the Rutland and Whitehall on May 1, 1871 and the lease of the line on June 15, 1871.
[1] The Castleton depot re-opened in 2010 and serves Amtrak's Ethan Allen Express.