The State Normal School was established in 1891 following decades of failed efforts in the Georgia legislature both to establish higher education for women and to expand upon the formal instruction of teachers. Only two years prior, the state had founded the Georgia Normal and Industrial College (present-day Georgia College and State University) in Milledgeville. The grounds on which the Athens Normal School was established had been occupied by a Confederate military school, called the University High School and located in a building commonly called Rock College, which as its name suggests was constructed out of rock quarried in Georgia. This school opened in 1862 and only operated for a few years, as Union soldiers took charge of the property upon the end of the war. In the years, 1866-1868, it was turned into a school for injured Confederate soldiers under the age of 30. After a short period being unused, the property became the home of the State College of Agriculture and Mechanic Arts (an independent institution, later to become the University of Georgia's College of Agriculture). The State Normal School opened in the summer of 1892 but permanent funding was not assured until 1894. Lawton B. Evans and Samuel D. Bradwell served as the first and second presidents, respectively, during these foundational years. Rock College was officially named Gilmer Hall, honoring George R. Gilmer (1790-1859) of Oglethorpe County, a Governor of Georgia (1829-1831; 1833-1835) who also served as a Representative in the U. S. Congress and the Georgia House; the Normal School was supported in part by the Gilmer Fund that had been established in his will.

The Normal School instructed those who were already working as teachers as well as those without prior experience. It offered a two-year program, with the first graduation exercises taking place in 1896. In 1903, the University of Georgia began providing additional training for teachers. These summer sessions were open to men and women, providing rare opportunities for women, as the University as a whole did not admit women until 1918. The University's School of Education opened in 1908. Meanwhile, the Normal School’s enrollment grew, and in turn the state provided additional funding, allowing for the construction of Bradwell Hall, the Auditorium, and the President’s Cottage. By the time President Bradwell retired in 1901, enrollment stood at roughly 600. Besides funding from the state and the Gilmer Fund, new donations from George Foster Peabody allowed for a significant expansion of the curriculum and the construction of Muscogee Hall. Moreover, the United Daughters of the Confederacy was responsible for the construction of Winnie Davis Hall. The organization wanted to honor the daughter of Jefferson Davis by building a home for young women students. Several new buildings were added in the 1910s as well: the Carnegie Library, Pound Auditorium (named for Jere Pound, the president of the school at that time), and Miller Hall. The previous auditorium became the Old Auditorium, but was later renamed George Hall.

The State Normal School became the Georgia State Teachers College (G. S. T. C.) in 1927. Since 1922, certain documents had referred to the institution as the State Normal College, as in that year it had begun offering a baccalaureate degree, a shift caused by higher standards for the education of teachers mandated by the state. In 1929, the school purchased the Cobb House, later known as Quarters A, a home that had been built in 1908. In 1932, upon the creation of the University System of Georgia, the University of Georgia absorbed the Georgia State Teachers College (as well as the aforementioned College of Agriculture and Mechanic Arts). After the 1932-1933 school year, the College of Education ceased holding classes at the Normal School campus, moving instead to Peabody Hall. The G. S. T. C. grounds became the Coordinate College, a junior college for women. The University also house a Demonstration School on the campus.

The U. S. Army leased the property during the nation’s involvement in the Second World War; because of decreased enrollment, the University did not need to house women students at the Coordinate College. A specialized training program was conducted during these years. After the war, though, the University again used the campus to house women students. In 1954, the United States Navy moved its Supply Corps School there from Bayonne, New Jersey, having purchased the property the previous year. In 2005, a round of Military base closures included the Supply Corps School, which relocated to Newport, Rhode Island. The Navy transferred ownership of the property to the University of Georgia on October 19, 2010. The Health Sciences Campus of the University of Georgia opened in 2012.