Cocaine, used by millions globally, creates feelings of reward by increasing dopamine in the brain. Chronic use can lead to cocaine use disorder (CUD), affecting about 20% of cocaine users, which is characterized by compulsive use and relapse that can be triggered by drug-related cues and contexts. Though research on substance use disorders has primarily focused on the mesolimbic reward pathway, the hippocampus (HPC) plays an important role in the spatial and contextual reward-associated learning. Specifically, the dorsal dentate gyrus (dDG) of the HPC is necessary for forming these contextual memories and contains dopamine D1 receptors (D1Rs) that are activated by cocaine-induced accumulation of dopamine. We investigated epigenomic and transcriptional changes in the dDG associated with cocaine contextual learning. First, we present large-scale changes in DNA methylation, primarily hypomethylation, after cocaine self-administration (SA), implicating the dDG and contextual encoding in a behavior primarily thought of as a cue-paired behavior. Next, we found hypomethylation after acquisition of cocaine conditioned place preference (CPP) a drug-paired contextual learning task. After cocaine CPP is acquired, the drug-associated memory can be extinguished through repeated exposure to the previously cocaine-paired environment in the absence of the drug. Finally, we report variability in extinction across genetically identical mice and corresponding DNA methylation differences, a potential epigenomic mechanism underlying these individual differences. The differentially methylated genes are primarily enriched in the calcium signaling pathway, demonstrating epigenomic changes in genes necessary for hippocampal learning that may help to elucidate differences between humans susceptible and resistant to developing CUD. Across these three behavioral paradigms, cocaine causes hypomethylation in regions enriched with enhancer-associated chromatin signatures that are also enriched with transcription factor binding motifs, providing a potential mechanism by which enhanced dopamine buildup by cocaine could alter the genomic landscape of the dDG to build strong drug-paired memories. Additionally, there is upregulation of genes necessary for the structural changes of learning and synaptic plasticity, that may also aid in the strong drug-associated learning. In sum, these findings highlight the importance of the dDG in cocaine-paired contextual learning and reveal underlying epigenomic and transcriptional changes caused by this type of learning.