Background: Group A Streptococcus (GAS) is a significant cause of both mild and life-threatening infections. While little is known about the role of DNA methylation in GAS, epigenetic control of gene expression through DNA methylation is an important regulator of growth, immune evasion, antibiotic resistance, and virulence in other bacterial pathogens1. GAS strains encode one major methylation system (HsdRSM)2, with individual strains possessing one of several recognition motifs. We sought to define the putative methylome of GAS at a species-wide level. Methods: A GAS pangenome was constructed in panaroo using 276 publicly available genomes. The methylation motif of the HsdRSM system was determined by BLAST comparison to enzymes with previously confirmed motifs. For each genome, the corresponding motif was annotated to give the putative methylome of the isolate. Functional analysis was performed using the ClusterProfiler R package. Results: The hsdRSM locus was intact in 270/276 isolates, with twelve unique methylation motifs identified. The mean number of methylation motifs per genome was 388.7 (range: 179-574). Principle component analysis of methylated genes in each genome produced four clusters. Three were single-motif clusters but contained multiple unrelated lineages, implying conserved methylation patterns. Despite all methylation motifs being present in more than one lineage, 43-67% of methylation sites were present in >95% strains sharing a given motif. The core methylome of three motifs were significantly enriched for genes encoding core metabolic functions (adjusted p<0.05). Conclusion: This work demonstrates conservation of methylation sites across genetically distant lineages, implying selective pressure on motif distribution.