Humans are exposed to a myriad of toxicants that have negative health consequences on generations to come. These generational effects first described in animal models and epidemiological studies, implicated germline epigenetic factors. Nonetheless, the molecular mechanisms mediating epigenetic inheritance remains almost entirely unexplored in humans. Exposure to the insecticide dichlorodiphenyltrichloroethane (DDT) is linked to birth defects, cancer, and neurodevelopmental delays. Although DDT has been banned world-wide since the 1970s, it is still sanctioned for indoor residual spraying to control malarial disease vectors in Sub-Saharan Africa. The impacts of DDT on human health are not only restricted to regions of use since DDT is transported over long distances to Arctic regions by ocean currents. Here, we studied two geographically diverse DDT-exposed populations, Greenlandic Inuit and South African VhaVenda men, and aimed to determine whether sperm DNAme and chromatin enrichments were associated with levels of DDT exposures and could be implicated in epigenetic inheritance. To quantitatively identify regions that were altered in DNAme and histone enrichment of exposed men, we used a sperm customized methyl-capture approach followed by sequencing (MCC-seq), and chromatin immunoprecipitation targeting histone H3K4me3 followed by sequencing (ChIP-seq). We then performed differential and functional analyses to investigate the relationship between DDT-associated alterations in the sperm epigenome, their predicted transmission to the embryo at fertilization, and persistence throughout development. We identified regions with altered DNAme (DNAme) and differential enrichment of H3K4me3 that were dose-like responsive to serum DDE levels. Altered sperm DNAme and H3K4me3 occurred at regulatory regions involved in fertility, disease, development and neurofunction. A subset of regions with altered sperm DNAme and H3K4me3 occurred at transposable elements and were predicted to persist in the pre-implantation embryo. These findings suggest that DDT exposure in men may negatively impact embryo development and the health of future generations through epigenetic mechanisms.