Interactions between plants and viruses have ecological and evolutionary implications for natural communities and present a potential threat for crops. However, virus diversity is not well characterized across wild plant hosts in natural habitats. Here, I present evidence that a common agricultural pathogen, Turnip mosaic virus (TuMV), is a prevalent viral symbiont for the widespread weedy plant Hesperis matronalis in upstate New York and beyond. High throughput sequencing of host and virus RNA confirms that TuMV infections are systemic and sufficient to induce color breaking floral phenotypes, which I then use to conduct image analysis of citizen scientist data and build a distribution model describing the biogeography of Hesperis-TuMV interactions across North America. Human modification of terrestrial environments is a key factor determining the presence of TuMV in H. matronalis, and I show that the Great Lakes and Upper Midwest regions of North America have the highest prevalence of TuMV infected H. matornalis hosts. Furthermore, my research demonstrates that H. matronalis genotypes are often tolerant to TuMV infection. Using stable isotope methods and life history traits to discern pre- versus post- reproductive fitness impacts of infection, this study indicates that there is likely selection for host tolerance in wild populations. This conclusion is supported by results of a classical G x E common garden experiment. Negative impacts of TuMV infection are slight across most host genotypes, and mortality occurred in only one experimental host family. Together, my research on the widespread TuMV-Hesperis pathosystem shows that humans impact the ecology and evolutionary trajectory of wild plant-virus interactions. In the final chapter of this dissertation, I present a participatory assessment of stakeholder priorities in Alaskan smallholder agriculture. Just as in wild plant systems, crops in high latitude regions are experiencing complex and irregular abiotic and biotic conditions. In order to understand what biological researchers can offer to knowledge-holders and practioners, it is critical to first listen and learn about the key issues they face. We lay the foundation for further participatory vegetable breeding efforts that may increase food and harvest security under changing environmental conditions.