Parasitoids are insects that use other insects as hosts. They sabotage host cellular and humoral defenses to promote the survival of their offspring by injecting viruses and venoms along with their eggs. Many pathogens and parasites disrupt host epigenetic mechanisms to overcome immune system defenses, and we hypothesized that parasitoids may utilize the same strategy. We used the ichneumon wasp Pimpla turionellae as a model idiobiont parasitoid to test this hypothesis, with pupae of the greater wax moth Galleria mellonella as the host. We found that parasitoid infestation involves the suppression of host immunity-related effector genes and the modulation of host genes involved in developmental hormone signaling. The transcriptional reprogramming of host genes following the injection of parasitoid eggs was associated with changes in host epigenetic mechanisms. The introduction of parasitoids resulted in a transient decrease in host global DNA methylation and the modulation of acetylation ratios for specific histones. Genes encoding regulators of histone acetylation and deacetylation were mostly downregulated in the parasitized pupae, suggesting that parasitoids can suppress host transcription. We also detected a strong parasitoid-specific effect on host microRNAs regulating gene expression at the post-transcriptional level. Our data therefore support the hypothesis that parasitoids may favor the survival of their offspring by interfering with host epigenetic mechanisms to suppress the immune system and disrupt development.