Opened in 1926 as the Jefferson City Junior College, the Miller Center has served a number of educational purposes through the years, including Jefferson City High School, Jefferson City Junior High School, and the Instructional Resource Center.

Besides housing the theater and the Railton Art Gallery, the Miller Center is also home to the Jefferson City Academic Center and the Jefferson City Public School District's Adult Education programs.

The renovated Miller Performing Arts Center opened October 5, 2005. The $4.5 million renovation was funded strictly through private donations of the the citizens and businesses of Jefferson City. The Miller Center is used for educational, community and professional arts programs.