Bark beetles are important agents of tree mortality in conifer forests and their interaction with trees is influenced by host defense chemicals, such as monoterpenes and phenolics. Since mountain pine beetle (Dendroctonus ponderosae Hopkins) has expanded its host range from lodgepole pine (Pinus contorta Doug. ex Loud. (var. latifolia Engelm.))-dominated forests to the novel jack pine (Pinus banksiana Lamb.) forests in western Canada, studies investigating the jack pine suitability as a host for this beetle have exclusively focused on monoterpenes, and whether phenolics affect jack pine suitability to mountain pine beetle and its symbiotic fungus Grosmannia clavigera is unknown. We investigated the phenolic and monoterpene composition in phloem and foliage of jack and lodgepole pines, and their subsequent change in response to water deficit and G. clavigera inoculation treatments. In lodgepole pine phloem, water deficit treatment inhibited the accumulation of both the total and richness of phenolics, but had no effect on total monoterpene production or richness. Fungal infection also inhibited the total phenolic production and had no effect on phenolic or monoterpene richness, but increased total monoterpene synthesis by 71%. In jack pine phloem, water deficit treatment reduced phenolic production, but had no effect on phenolic or monoterpene richness or total monoterpenes. Fungal infection did not affect phenolic or monoterpene production. Lesions of both species contained lower phenolics but higher monoterpenes than non-infected phloem in the same tree. In both species, richness of monoterpenes and phenolics was greater in non-infected phloem than in lesions. We conclude that monoterpenes seem to be a critical component of induced defenses against G. clavigera in both jack and lodgepole pines; however, a lack of increased monoterpene response to fungal infection is an important evolutionary factor defining jack pine suitability to the mountain pine beetle invasion in western Canada.