At the time of its closure, Castleton had an enrollment of 2000 students and offered more than 30 undergraduate programs, as well as master's degrees.

Castleton University traced its history to the Rutland County Grammar School, chartered by the Vermont General Assembly on October 15, 1787.

Principal Solomon Foot (1826–1829), who would go on to be President pro tempore of the U.S. Senate during the Civil War, was the driving force in this expansion of the school.

For 30 years the Normal School property and grounds were privately owned by Abel E. Leavenworth and his son Philip.

She hired staff with advanced degrees, and broadened her students' exposure to the world by bringing people such as Helen Keller, Robert Frost, and Norman Rockwell to Castleton.

[16] On July 23, 2015, the Vermont State Colleges Board of Trustees voted unanimously to change the name of the institution to Castleton University.

[17] Nearby Rutland plays host to the Castleton Polling Institute, as well as a professional development center for educators and entrepreneurs.

In September 2016, the university opened Foley Hall, a two-floor residence, in collaboration with Green Mountain Power and Efficiency Vermont that provides housing for students.

The institute's founding director, Rich Clark, a professor of political science, had been working in academia and polling for 15 years before coming to Castleton in 2011 from the University of Georgia.