The Manlius School was founded in 1869 in Manlius, New York as the St. John's School. However, by 1880 attendance had fallen to the point where the school became insolvent. As a result, in 1881 it was reorganized as the St. John's Military School.

By 1887 the reorganized St. John's again found itself with enrollment and financial problems, and the trustees looked for someone who could not only turn the school around, but also assume all financial risks. This person was General William Verbeck, who at the time was the co-principal of a military academy in Aurora, NY. By the time of his death in 1930, what was now known as The Manlius School had become one of the top military schools in the United States.
His son, Guido Verbeck, who had been associated with the school for many years, then became the head of school. Guido died in July 1940.

By the late 1960s enrollment at military schools was falling off as more and more people became disenchanted with the Vietnam War. The Manlius School did not escape this trend, and once again financial difficulties were on the horizon. At the same time, Pebble Hill was running out of room for the many students who were enrolled there. In 1970 the two schools merged to become Manlius Pebble Hill School.

At first the newly merged school used both campuses, with the DeWitt campus being used for the Lower School and Middle School and the Manlius campus used for the Upper School. However, by 1973 it became impractical to run two campuses. The Manlius campus was shut down beginning with the 1973-74 school year and all classes were moved to the DeWitt campus; the MPH Class of 1974 was the last class whose commencement was in Knox Hall on the Manlius campus. The Manlius campus was sold in 1979 to a private developer.

The "Old Boys of Manlius" as the school's alumni were known, served in a number of wars including World War I, World War II, Korea and Vietnam.