Infections caused by alphaviruses, including chikungunya virus (CHIKV), exhibit considerable variation in disease outcomes, influenced by host factors. Among these, age is a key determinant. This project aims to understand the age-related determinants which drive differences in infection outcomes. Although age-related susceptibility to alphaviruses is well documented, the non-immune mechanisms behind these differences remain poorly understood, with current explanations largely focused on systemic immune factors. In this study, we used an established immunocompetent mouse model to study differences in CHIKV susceptibility during early development. We found that C57BL6/J mice showed an age-dependent susceptibility, with younger mice exhibiting higher viremia and more severe joint inflammation. Early during infection, enhanced viral tropism was observed within the non-immune compartment of the joint footpad, with non-immune cells in younger mice exhibiting higher susceptibility to infection. Multi-omic profiling further revealed cell-type specific, age-related rewiring of lipid signalling pathways, implicating these pathways in driving differential CHIKV susceptibility. Inhibition of these pathways reduced CHIKV infection in non-immune cells isolated from the joint footpad in vitro and similarly led to decreased viremia and joint inflammation in vivo. Together, these findings highlight a previously underappreciated role for non-immune, tissue-intrinsic factors in disease pathogenesis and provide a foundation for developing targeted interventions to mitigate arboviral disease severity in vulnerable populations.