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Abstract Diverse geographic, environmental, and ecological factors affect gene flow and adaptive genomic variation within species. With recent advances in landscape ecological modelling and high‐throughput DNA sequencing, it is now possible to effectively quantify and partition their relative contributions. Here, we use landscape genomics to identify determinants of genomic differentiation in the forest tent caterpillar, Malacosoma disstria, a widespread and irruptive pest of numerous deciduous tree species in North America. We collected larvae from multiple populations across Eastern Canada, where the species experiences a diversity of environmental gradients and feeds on a number of different host tree species, including trembling aspen (Populus tremuloides), sugar maple (Acer saccharum), red oak (Quercus rubra), and white birch (Betula papyrifera). Using a combination of reciprocal causal modelling (RCM) and distance‐based redundancy analyses (dbRDA), we show that differentiation of thousands of genome‐wide single nucleotide polymorphisms (SNPs) among individuals is best explained by a combination of isolation by distance, isolation by environment (spatial variation in summer temperatures and length of the growing season), and differences in host association. Configuration of suitable habitat inferred from ecological niche models was not significantly related to genomic differentiation, suggesting that M. disstria dispersal is agnostic with respect to habitat quality. Although population structure was not discretely related to host association, our modelling framework provides the first molecular evidence of host‐associated differentiation in M. disstria, congruent with previous documentation of reduced growth and survival of larvae moved between natal host species. We conclude that ecologically mediated selection is contributing to variation within M. disstria, and that divergent adaptation related to both environmental conditions and host association should be considered in ongoing research and management of this important forest pest.

Abstract Temporal separation of reproductive timing can contribute to species diversification both through allochronic speciation and later reinforcement of species boundaries. Such phenological differences are an enigmatic component of evolutionary divergence between two major forest defoliator species of the spruce budworm complex: Choristoneura fumiferana and C. occidentalis. While these species interbreed freely in laboratory settings, natural hybridization rates have not been reliably quantified due to their indistinguishable morphology. To assess whether temporal isolation is contributing to reproductive isolation, we collected adult individuals throughout their expected zone of sympatry in western Canada at 10‐day intervals over two successive years, assigning taxonomic identities using thousands of single nucleotide polymorphisms. We found unexpectedly broad sympatry between C. fumiferana and C. occidentalis biennis and substantial overlap of regional flight periods. However, flight period divergence was much more apparent on a location‐by‐location basis, highlighting the importance of considering spatial scale in these analyses. Phenological comparisons were further complicated by the biennial life cycle of C. o. biennis, the main subspecies of C. occidentalis in the region, and the occasional occurrence of the annually breeding subspecies C. o. occidentalis. Nonetheless, we demonstrate that biennialism is not a likely contributor to reproductive isolation within the species complex. Overall, interspecific F1 hybrids comprised 2.9% of sequenced individuals, confirming the genomic distinctiveness of C. fumiferana and C. occidentalis, while also showing incomplete reproductive isolation of lineages. Finally, we used FST‐based outlier and genotype–environment association analyses to identify several genomic regions under putative divergent selection. These regions were disproportionately located on the Z linkage region of C. fumiferana, and contained genes, particularly antifreeze proteins, that are likely to be associated with overwintering success and diapause. In addition to temporal isolation, we conclude that other mechanisms, including ecologically mediated selection, are contributing to evolutionary divergence within the spruce budworm species complex.