Prostate cancer (PCa) aggressiveness is ancestry dependent. Specifically, men of African ancestry are disproportionately impacted, including a 3- to 5-fold increased risk for mortality compared with European or Asian men, respectively. Not explained by socioeconomic factors alone, clearly environment, biology and genomics, including epigenomics, are at play. While it is understood that DNA methylation alterations drive PCa initiation and progression, the role of epigenetic aberrations associated with PCa ethnic disparities remains elusive. However, lack of African relevant data and European-biased informatic workflows have hindered progress. Addressing these limitations, we generate not only a unique African-inclusive multi-ethnic prostate tumour-derived genome-wide methylation resource (56 African, 49 European and 22 Asian), but establish an Illumina EPICv1 and EPICv2 African-relevant epigenomic filtering resource. Observing little differential DNA methylation between Australian-derived European and Asian tumours, in contrast African tumours showed significant heterogeneity – echoing the population’s vast genomic diversity. Notably, African over non-African tumours showed more hypermethylated sites (721 versus 140), with notable enrichment of regulatory enhancers (342 CpGs, 39.72%). While typical candidates such as GSTP1, APC and RARB were absent, significant differentially methylated positions (DMPs) and regions (DMRs) include 15 novel African-specific PCa targets. Further comparative analysis for 58 tissue-matched African controls showed greater tumour-associated heterogeneity and elevated hypermethylation (31,051 versus 22,263 sites), again with enhancer enrichment (19,452 CpGs, 36.49%). Putative enhancer interactions in African-derived prostate tumours highlight the potential significant impact these regulatory intergenic regions have on PCa-associated ethnic disparities. Besides six additional novel PCa targets, we found olfactory transduction pathway genes to be significantly enriched. While ectopic expression is recognized in prostate carcinogenesis, this is the first study to suggest this pathway to be epigenomically altered in PCa, with African specificity. To the best of our knowledge, this is the first African-inclusive multi-ethnic approach providing epigenomic insight into PCa ethnic disparities.