Ross River virus (RRV) is a mosquito borne arbovirus that is capable of causing considerable human morbidity; associated with debilitating polyarthritis. RRV circulates annually and is thought to primarily be maintained in Australia in native macropod hosts, however humans and horses may play a significant role during epidemic activity. Although occurring widely in Australia and the Pacific region, record numbers of RRV case notifications (>2000) were reported during the 2016-2017 arbovirus season in Victoria. Additionally, virus transmission is suspected to have occurred in Melbourne, representing a rare event. Currently, we lack an understanding of the possible movement and dynamics of RRV in Australia. The Victorian Arbovirus Disease Control Program, a Victorian Department of Health and Human Services funded program run by Agriculture Victoria, utilises a tripartite approach to monitor and assess arboviral activity and risk. This approach comprises virological surveillance in mosquitoes, monitoring adult mosquito prevalence and veterinary surveillance. Through this program, 26 isolates of RRV were obtained during the 2016-2017 season, with these viruses largely isolated from Cx. annulirostris and Ae. camptorhynchus. Twenty-three of these isolates were from inland northern Victoria between Mildura (North-West) and Cobram (North-East). Two isolates were from Gippsland (South East) and a single isolate from Melbourne. Whole genome sequencing was performed for five spatio-temporally segregated isolates. Genomic analysis, using both recent and historical isolates from multiple hosts, show that the mosquito-derived isolates from Victoria in 2016–2017 were closely related to human RRV isolates collected since 2004, and were distinct to historic isolates from natural animal reservoirs. Although sequences of human RRV isolates from this epidemic were not available, our study suggests the endemic circulation of a high diversity of RRV in mosquitoes in the region that potentially contributed to human cases, emphasising the value of mosquito Xenosurveillance to capture the evolving viral ecology of RRV.