Environmental changes and phenotypic responses are directly linked through epigenetics - the cellular mechanism that switches genes on or off. In natural populations, the ability to rapidly change gene-expression determines how a species can cope with environmental extremes. Such plastic responses are crucial for populations to persist in the initial stages of adaptation. Here, we focus on DNA methylation of CpG dinucleotides, one of the main epigenetic modifications in vertebrates. We measured methylation changes in School Sharks (Galeorhinus galeus) that were subjected to different experimental conditions and examined (epi)genetic variation in natural populations. We sequenced 127 School Sharks to characterize 1.2 million CpG sites and 45,000 SNPs. In juvenile sharks subjected to acute thermal and salinity stress, we identified 208 CpG sites associated with these environmental stressors, indicating rapid methylation changes can provide a buffer to acute stress. Subsequently, we investigated these stress-related methylation patterns in natural population to understand if wild sharks show similar responses. We also studied the stability of methylation between tissue types. Overall, the study provides estimates of methylation and nucleotide diversity as a proxy for the adaptive potential of populations and highlight the use of epigenetic sequencing to monitor climate stress in wild animals.