Jamestown was first settled in 1754 by the Mendenhall family. It was a thriving community of craftsmen and had a strong Quaker presence. Education was a prime concern of residents of the Jamestown area from its earliest years. Subscription schools; a free night school for anyone who wished to "read, write and cipher;" a seminary for young ladies; Jamestown Female College, an academy; a law school and a medical school all flourished in the early years.

In 1885 the Guilford County Board of Education was organized for the improvement of instruction and educational advantages and a public school was conducted at this time in Old Jamestown.

In 1907 the North Carolina General Assembly enacted a law providing for the creation and maintenance of public high schools in each county. Jamestown Public School, a union school, was built and became the "best equipped school" in Guilford County with dormitories for boarding students. In 1914 the school was destroyed by fire, but a new building was completed the next year. This building now stands in the heart of Jamestown and houses the Jamestown Public Library.

The school grew steadily and a new high school complex in Jamestown was opened in September 1959. The new high school was named for Lucy Coffin Ragsdale because of her dedication and interest to public school education in Jamestown. The first principal of Ragsdale High School was T.G. Madison, followed by Dr. Steve Dalton. Dr. Kathryn Rogers, the current principal, is only the third principal in the history of the school.

Ragsdale has been accredited by the Southern Association of Colleges and Schools since 1962. Ragsdale was the first high school in Guilford County to receive this recognition.