Gene body methylation (GBM) is a taxonomically widespread epigenetic modification of the DNA the function of which remains unclear 1,2. GBM is bimodally distributed among genes: it is high in ubiquitously expressed housekeeping genes and low in context-dependent inducible genes 2,3, and it has been hypothesized that changes in GBM might modulate responses to environmental change, including transgenerational plasticity 4,5. Here, we profiled GBM, gene expression, genotype, and fitness characteristics in clonal fragments of a reef building coral Acropora millepora reciprocally transplanted between two distant reefs. We find that genotype-specific GBM is considerably more stable than gene expression and responds to transplantation predominantly by genome-wide increase or decrease in disparity of methylation levels among genes. A proxy of this change, GBM difference between the two gene classes (housekeeping vs. inducible), was the most important determinant of genomewide GBM variation in our experiment, explaining 33% of it. Surprisingly, despite apparent lack of capacity for environmental specificity, this simple genome-wide GBM adjustment was a good predictor of broad-scale functional shifts in gene expression and of fragments’ fitness in the new environment, which supports GBM’s role in acclimatization. At the same time, constitutive differences in GBM between populations did not align with plastic GBM changes upon transplantation and were mostly observed among FST outliers, indicating that they arose through genetic divergence rather than through transgenerational inheritance of acquired GBM states. We propose that during acclimatization GBM acts as a “single-knob equalizer” to rapidly achieve coarse genome-wide adjustment of gene expression, after which further finetuning is provided by expression plasticity of individual genes and longer-term genetic adaptation of both GBM and gene expression to local conditions.