Host plants provide resources critical to viruses and the spatial structuring of plant communities affects the niches available for colonisation and disease emergence. However, large gaps remain in the understanding of mechanisms that govern plant-virus disease ecology across heterogeneous plant assemblages. We combine high-throughput sequencing, network, and metacommunity approaches to test whether habitat heterogeneity in plant community composition corresponded with virus resource utilisation traits of transmission mode and host range. A majority of viruses exhibited habitat specificity, with communities connected by key generalist viruses and potential host reservoirs. There was an association between habitat heterogeneity and virus community structuring, and between virus community structuring and resource utilisation traits of host range and transmission. The relationship between virus species distributions and virus trait responses to habitat heterogeneity was scale-dependent, being stronger at finer (site) than larger (habitat) spatial scales. Results indicate that habitat heterogeneity has a part in plant virus community assembly, and virus community structuring corresponds to virus trait responses that vary with the scale of observation. Distinctions in virus communities caused by plant resource compartmentalisation can be used to track trait responses of viruses to hosts important in forecasting disease emergence.