Bark beetles are major causes of conifer mortality worldwide. We quantified genetic contributions to key chemical and physical traits in lodgepole pine that contribute to defense against mountain pine beetle, a native tree-killing herbivore. Assays were conducted with mature trees in replicated provenance trials. Among chemical defenses, monoterpene composition (relative proportions of various compounds) had higher genetic variability than monoterpene concentration (absolute quantities). Additionally, constitutive concentrations had higher genetic variabilities than induced concentrations elicited by simulated attack. Resin flow elicited by mechanical wounding likewise showed very low genetic variability. In previous studies with this and related systems, induced monoterpene concentration and resin flow are the two best predictors respectively of which trees will survive outbreaks under natural conditions. This means that expression of the most efficacious defense traits is strongly influenced by environmental factors. These low heritabilities despite their survival values likely arise from specific life history and ecological aspects of this system, such as the lengthy period between when lodgepole pines begin cone production and become large enough for brood development, the extended viability of serotinous cones post-mortem, the high heterogeneity of both resources and stressors that trees experience across landscapes, and a strong proximate-neighbor effect on tree mortality arising from beetle aggregation pheromones. However, low heritability values do not preclude long-term evolvability and coadaptation of defenses, for which there is extensive mechanistic and associational evidence in this system. Among other traits we evaluated, sesquiterpenes had higher genetic variability than monoterpenes. Sesquiterpenes are not known to influence conifer-bark beetle interactions but have anti-herbivore properties in some other plant-insect systems. The lengths of lesions formed in response to simulated attack showed no heritable component and likewise do not predict tree survival in nature. Bark texture was highly heritable and is known to influence beetle post-landing orientation and colonization patterns, but whether it influences survival patterns at the whole-tree level is unknown. Relationships between tree defenses and growth were generally positive, suggesting that environmental heterogeneity in resource quality among trees supersedes potential underlying substrate allocation processes within trees. Similarly, relationships between various defense traits were generally positive rather than showing trade-offs, suggesting conifer resistance to native bark beetles entails coordinated defense syndromes. Implications to tree breeding, forest management, and coevolution between long-lived plants and rapidly reproducing herbivores are discussed. The extent to which these trends may apply to other bark beetle systems is evaluated, along with specific priorities for future research.