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ABSTRACT Herbivorous insects tolerate chemical and metabolic variation in their host plant diet by modulating physiological traits. Insect immune response is one such trait that plays a crucial role in maintaining fitness but can be heavily influenced by variation in host plant quality. An important question is how the use of different host plants affects the ability of herbivorous insects to resist viral pathogens. Furthermore, the transcriptional changes associated with this interaction of diet and viral pathogens remain understudied. The Melissa blue butterfly (Lycaeides melissa) has colonised the exotic legumeMedicago sativaas a larval host within the past 200 years. We used this system to study the interplay between the effects of host plant variation and viral infection on physiological responses and global gene expression. We measured immune strength in response to infection by the Junonia coenia densovirus (JcDV) in two ways: (1) direct measurement of phenoloxidase activity and melanisation, and (2) transcriptional sequencing of individuals exposed to different viral and host plant treatments. Our results demonstrate that viral infection caused total phenoloxidase (total PO) to increase and viral infection and host plant interactively affected total PO such that for infected larvae, total PO was significantly higher for larvae consuming the native host plant. Additionally,L. melissalarvae differentially expressed several hundred genes in response to host plant treatment, but with minimal changes in gene expression in response to viral infection. Not only immune genes, but several detoxification, transporter, and oxidase genes were differentially expressed in response to host plant treatments. These results demonstrate that in herbivorous insects, consumption of a novel host plant can alter both physiological and transcriptional responses relevant to viral infection, emphasising the importance of considering immune and detoxification mechanisms into models of evolution of host range in herbivorous insects.