Eusocial insect colonies divide behaviors among specialist groups called castes. In some species, caste identity is determined by the interaction of endogenous (e.g. genomic) and exogenous (e.g. juvenile hormone from nurses) signals during larval development, suggesting epigenetic mechanisms underlie plastic traits tied to caste identity. Previous work demonstrated a link between patterns of histone H3 lysine 27 acetylation (H3K27ac) and caste-specific gene expression in Major and Minor workers of the ant Camponotus floridanus, and we hypothesized caste-specific behaviors such as foraging may be similarly regulated by histone acetylation. To test this hypothesis, we fed mature (~30d old) Majors and Minors with histone deacetylase inhibitors (HDACi), and CBP-dependent histone acetyl transferase inhibitors (HATi). We observed foraging enhancement after HDACi, and foraging suppression after HATi in Minors. Curiously, we did not observe increased foraging in HDACi treated mature (~30d) Majors. However, HDACi injections in callow (0-1d old) Majors succeeded in causing stable reprogramming of foraging behavior, indicating a critical period, or ‘window’ of epigenetic sensitivity to HDACi exists in young majors. To address this possibility, we injected Majors with HDACi in a time course and observed juvenile (d0-d5) Majors are susceptible to reprogramming, whereas mature (d10) Majors are not. To assess innate differences in the brain between castes, we conducted an RNA-seq study in untreated Major and Minor workers 0, 5, and 10 days old, and detected caste-specific patterns of juvenile hormone and ecdysone signaling. Finally, to characterize the transcriptional and epigenetic effects of reprogramming, we conducted RNA-seq in HDACi treated Major brains, and detected consistent upregulation of members of the neuron restrictive silencing factor (NRSF/REST) repressive complex (e.g. CoREST, RPD3, ttk). Notably, the top downregulated gene after HDACi is juvenile hormone esterase (JHe), which antagonizes JH signaling and inhibits foraging behavior in many eusocial insects. Thus, our results suggest REST/CoREST mediated repression of JHe may be a significant source of stable changes to foraging in behaviorally reprogrammed Majors.