Identifying the putative environmental factors that influence the adaptive outcomes ofpopulations as they respond to heterogeneity remains a major focus of evolutionary biology. The ability to observe the genomic and phenotypic evolution of populations over rapid timescales has enabled a deeper exploration into the role particular environmental variables have on a population’s response to selection. While replicate populations of Drosophila melanogaster adapt to natural seasonal variation in an ecologically relevant context, we perturb elements of the resource and microbial environment to observe the effects of this environmental variation on host ecology, evolution, and microbial association. We determine that changes in the resource and microbial environment alter the adaptive trajectories of population phenotype and genotype, with this effect being consistent across replicates. Adaptation to the resource environment was trait-specific and exhibited an oligogenic architecture, while the response to the season was genome-wide and observed across all traits. Adding two distinct resident microbial taxa to the host’s environment elicited similar effects on traits between the two treatment groups, while diverging significantly from control populations. Significant distinctions between microbial taxa treatments were evident only at the genomic level. Additionally, we describe elements of the population and its environment that shape host-microbial associations over seasonal time, which may indirectly influence host evolution by modifying these microbial associations. Finally, we describe co-adaptive dynamics between the host and their microbial community by determining that microbial-mediated trait plasticity can evolve rapidly, and populations express distinct trait values when assayed with the microbial community derived from their population. We conclude that populations can simultaneously adapt to various environmental factors, with seasonal environmental shifts consistently serving as the primary driver of trait and genomic variations. These results highlight the impact of ecological processes on evolutionary outcomes and encourage further investigation into eco-evo feedback dynamics between host and microbial communities. Natural populations experience frequent heterogeneity as they persist through abiotic environmental change, cycles of resource availability, and microbial community variation; the impact of these sources of variation on populations likely contributes to the maintenance of genetic diversity and may influence patterns of local adaptation and speciation.