Host-parasite interactions are extremely important drivers of evolutionary change, characterised by co-evolutionary dynamics with strong reciprocal selective pressure on both host and parasite genomes. However, little is known about the genomic basis of host-parasite interactions, particularly which genes may affect parasite susceptibility, parasite burden and the ability to resolve energetic life-history trade-offs under chronic parasite insult. This thesis examines the genomic, epigenomic and transcriptomic basis of an avian host's physiological response to chronic parasite infection. The model system throughout is the red grouse (Lagopus lagopus scotica) and its main parasite, the gastrointestinal nematode Trichostrongylus tenuis. T. tenuis is highly prevalent and imposes substantial fitness costs that affect demography and population dynamics through an impact on territorial behaviour, energy balance, fecundity and mortality. Here, the genomic architecture of variation in individual T. tenuis burden is examined via de novo identified candidate genes, genome-wide SNPs and genome-wide cytosine methylation polymorphisms. Further, molecular signatures of natural selection in identified genomic regions are examined across a landscape in northeast Scotland with heterogeneous parasite pressure. Finally, the transcriptomic response of red grouse to experimental T. tenuis infection and manipulation of testosterone titre is harnessed to identify a transcriptomic component in testosterone-driven physiological trade-offs in a sexual selection context.