Trait development exists in an ecological context, subject to the surrounding environment and its abiotic and biotic stimuli. Traits respond to external pressures through mechanisms that either buffer their effects or leverage them as signals to change the trajectory of development. Variation in the mechanisms that make trait development robust or plastic can affect population persistence and selection by changing the distribution of phenotypes within a population. The epigenetic factors that make developmental mechanisms plastic and the causes of variation in plastic traits are poorly understood in natural populations. In this dissertation, I test three key hypotheses about the development and evolution of seasonally plastic traits. In chapter one, I test the hypothesis that environmentally sensitive temporal windows of development are defined by epigenetic changes to chromatin accessibility that are driven by endocrine signals. I test this hypothesis by manipulating endocrine signals ex-situ in buckeye butterfly (Junonia coenia) wings, quantifying the transcriptional and epigenetic response across development, and performing targeted gene deletion of endocrine-responsive loci. I find that loci involved in the development of plastic traits are activated by endocrine signals that indirectly change regulatory element accessibility. Binding sites for chromatin remodeling proteins are therefore likely to be key determinants of whether traits are sensitive to environmental cues. In chapter two, I test whether canalized phenotypic plasticity is accompanied by similar decreases in gene expression and epigenetic plasticity. I quantified gene expression and chromatin accessibility in the developing wings of butterflies from two populations that differ in their degree of wing color plasticity and find that the population with less phenotypic plasticity exhibits greater levels of transcriptional plasticity. Key genes involved in plastic color pattern development are plastically expressed in the canalized population, suggesting that this population might have evolved a mechanism to buffer the effects of environmental stimuli on wing development. In chapter three, I test whether variation in the degree of plasticity in multiple, coordinated traits is genetically coupled. Using a GWAS, in-situ hybridization, CRISPR, and gene expression and chromatin accessibility data from Ch. 2, I find that plastic traits are both developmentally and evolutionarily modular, which could permit plasticity to be readily tailored to local environmental conditions.