The fungus, Batrachochytrium dendrobatidis (Bd), aetiological agent of the devastating amphibian skin disease chytridiomycosis, is now considered endemic in most climatically suitable regions around the world. The evolution of or assisted selection for host immune resistance to chytridiomycosis may be a promising avenue for ensuring sustainable long-term persistence of Bd-threatened wild amphibians. For such a strategy to succeed it is essential to understand the mechanisms by which such resistance manifests. Here we examined transcriptomic responses of alpine tree frogs (Litoria verreauxii alpina) to subclinical Bd infection, comparing long-exposed populations to a naïve population. We performed a blinded, randomized and controlled exposure experiment, collecting skin, liver and spleen tissues at 4, 8 and 14 days post-exposure from 51 frogs for transcriptome assembly and differential gene expression analyses. We analysed our results in conjunction with data on infection intensities and the results of a large clinical survival experiment run concurrently in the same species. We identified a large number of significantly dysregulated transcripts (liver 1043, skin 8165, spleen 1665) in the tissues from subclinically infected individuals versus unexposed negative control frog tissue, including the predominant up-regulation of numerous transcripts associated with the host immune response (liver 132, skin 645, spleen 216). Our comparison between populations highlighted variations in response to subclinical infection associated with long-term population Bd exposure history and clinical evidence of survival. Individuals from the longest-surviving population demonstrated a larger complement of differentially expressed immune-associated genes in the skin at 4 days post exposure than frogs from the two more susceptible populations, consistent with a robust early innate and adaptive immune response. Our results support the concept of selecting for the evolution of resistance against chytridiomycosis, and suggest that an insufficient early immune response to infection may contribute to the susceptibility of this non-model species to chytridiomycosis.