The skin is the first line of defence against most infections, including those by arthropod-borne viruses (arboviruses) such as Ross River virus (RRV) and Chikungunya virus (CHIKV). RRV and CHIKV are arthritogenic arboviruses that cause debilitating musculoskeletal and arthritic disease. They are considered significant public health threats of major global concern due to the scale of outbreaks, and the limited treatment options available. The skin is a compartmentalised organ and is populated by an abundance of immune and non-immune cells which have been proven targets of mosquito-borne viruses. To understand the dynamics of arthritogenic arbovirus dissemination following skin infection, we developed a pathogenic model of RRV infection to mimic a mosquito bite. We demonstrated that inoculation of RRV intradermally into the skin of mice disseminates systemically to causes musculoskeletal pathogenesis similar to that observed for the current subcutaneous RRV infection model. Further, we provide evidence suggesting RRV disseminates from the site of infection in the skin to lymphoid organs via lymphatic drainage at earlier stages of infection (prior to 24hpi). Consistent with cutaneous arboviral infection studies, we found inflammatory monocytes, neutrophils and dermal macrophages dominated the early inflammatory response in the skin. Importantly, we unveiled a critical role for cellular source of the virus in driving viral dissemination kinetics and disease severity. Intradermal infection with RRV derived from mosquito cells resulted in more severe disease compared to RRV derived from mammalian cells. This difference in disease was accompanied by specific transcriptional responses to mammalian cell-derived RRV and mosquito cell-derived RRV in the skin and skin draining LN after intradermal infection. Interestingly we show evidence indicating that cellular source of the virus dictates the dissemination of RRV to target tissues in muscle and joint. Finally, we used our intradermal infection model to elucidate a role for RRV envelope glycosylation in determining the differences in disease severity between mosquito cell and mammalian cell-derived RRV. Using glycan mass spectrometry and Nanostring differential gene expression analysis, we show that the high mannose N-linked glycans on RRV derived from mosquito cell aid virus to evade immune detection to replicate efficiently and establish increased dissemination of RRV leading to a more severe disease. Using a physiologically relevant model of cutaneous arboviral infection, we show previously unappreciated mechanisms of immune response and viral dissemination that, in future, will help develop novel approaches to limit arboviral dissemination and ameliorate disease outcomes.