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In 1949 the main part of the present school site was purchased by the NSW Government for the purpose of Agricultural Education. The school that commenced on this site in 1956 was an annex of Carlingford District Rural School with Charles Mullavey as the Master in Charge. At that time the school consisted of a wooden five room classroom block, a small staffroom and male only ablution facilities. By the start of 1958 the school was independent of Carlingford District Rural School and was called the "Carlingford Junior Agricultural High School" (the Junior part of the name reflected the fact that students at that time could only undertake the first three years of their secondary education at the school).
In 1959 the name of the school was changed to "Carlingford Agricultural High School" (to reflect its new full high school status - although there were no actual Fourth and Fifth Year classes at that time). The first Headmaster, James C. Hoskin, and his Deputy Headmaster, Charles Mullavey, commenced duties at the start of that year and in April, the name of the school changed again - this time to "James Ruse Agricultural High School".
When James Hoskin was studying Agricultural History in University, he had been interested in James Ruse due to his significance in the early development of agriculture in Australia, and also because "both Ruse and I [Hoskin] are of Cornish extraction". Mr Hoskin questioned the name of the school (Carlingford Agricultural High School) as the school was not serving just the Carlingford area (in fact there were only a small number of students from Carlingford). In April 1959 Mr. Hoskin put forward a proposal to the then New South Wales Department of Education outlining two new names for the school: Sydney Agricultural High School and Ruse Agricultural High School; eventually, the Department agreed to a modification of the latter.
Hoskin soon became synonymous with the school, as he served as headmaster until his retirement at age of 65 in 1978. During this time, the school became established as one of the few public schools that were selective; initially because of its agricultural speciality, then for its reputation as a quality school. For his efforts, Hoskin was awarded the Queen's Silver Jubilee Medal in 1977 and the Order of Australia for Services to Education in 1990.
The first group of students to complete the full five years of secondary education at the new high school sat for the Leaving Certificate in 1961. Most of these boys were part of the initial enrolement of 1st Year pupils at the Felton Rd. site, in 1957. James Ruse AHS was originally a boys only school, but gradually became co-educational after an initial intake of 24 female students into Year 11 in 1977.
Since the mid 1990s, James Ruse has undergone an extensive building works program funded by both parents of students and the State and Federal Governments. 1997 saw the completion of Stage 1 of this program (encompassing a new Library block and English classrooms which replaced the old Anderson building, a new block containing Art and HSIE classrooms, the integration of the existing Powe block and the former library into a science block, and the installation of an elevator in the Perrau block to improve wheelchair accessibility).
In 2000, Stage 2 of the program began with the first building (a 180 seat lecture theatre) completed in early 2001. The Schofield block became part of the program in 2002 after the building was damaged by arson. During the next two years the old Technology Block and the Francis block were demolished due to a white ant infestation, with both blocks being rebuilt and refurnished in 2004. The final stage of the works were underway at the time of the departure of Principal Michael Quinlan, who retired in 2006 after having been Principal since 1992.