Ross River virus (RRV) infection is the most frequently notified arboviral disease in Australia with approximately 5500 cases reported annually over the past decade. The prototype strain of RRV (T48) was isolated in 1959 from Aedes vigilax mosquitoes trapped beside the Ross River in Townsville, Queensland. Since then, outbreaks have been recorded in every Australian state as well as the South Pacific and Western Pacific regions. We sequenced the complete genome of three RRV strains isolated from infected ADF personnel and mosquitoes captured in ADF training areas. The complete nucleotide sequences comparison revealed remarkable conservation between 1959 and 2018 with a maximum divergence of only 3.9% genome wide. Phylogenetic analysis of RRV E2 and nsP3 nucleotide sequences between 1959 and 2018 show that the Most Recent Common Ancestor (MRCA) of RRV existed about 90 years ago and gradually evolved into three distinct evolutionary populations. The RRV virus in lineage I and II were isolated from either birds or mosquitoes but viruses in these lineages have not been sampled since 1979 and 1991, respectively. These two lineages appear to have become extinct and, we hypothesise, were displaced by lineage III which, collectively, have been responsible for every RRV outbreak over the last 40 years. The MRCA for RRV in lineage III was discovered in 1979 and it has evolved into seven sublineages since then. An analysis of the RRV E2 protein sequence revealed three common sites for amino acid substitution (Tyr18His, Ile67Leu and Arg251Lys) between current circulating lineage III and the prototype strain T48. These sites have a significant influence on the structural and electrostatic composition of the E2 protein and may have contributed to the supplantation of earlier lineages with those circulating today.