The telomere repetitive TTAGGG motif at the ends of chromosomes serves to preserve genomic integrity and chromosomal stability through telomerase or alternative lengthening of telomeres mechanisms. In turn, genomic instability is a hallmark of cancer—implicating telomere disturbance. Prostate cancer (PCa) shows significant ancestral disparities, where we have found shortened tumour telomere length to be associated with aggressive PCa presentation and elevated genomic instabilities in men of African over European ancestry. Yet, no study has explored the contribution of inherited variation in genes controlling for telomere maintenance (TelGenes) with respect to ancestrally driven PCa disparity. Focusing on 1016 TelGenes, we interrogated for common PCa risk association using an African-specific case-control exomic array (451 cases, 292 controls) and for rare pathogenic variants using a multi-ethnic whole genome sequenced PCa resource (117 African, 62 European). Identifying 17 TelGene PCa risk alleles, while associating 7 alleles with aggressive disease presentation (203 high-risk, 476 low-risk/controls) in African, notably, none of these risk alleles are known to European-biased PCa studies. Notably, the top risk candidates identified in BCR (rs35537221) and ESR1 (rs12154178), where the genes have previously been associated with leukemia/lymphoma and breast cancers, respectively. Conversely, the top aggressive disease associated variant impacting the histone linker gene H1-5 (rs11970638), is a known tonsil cancer risk allele. Using African and European-specific workflows, 18 and 21 pathogenic TelGene variants were identified, respectively, with one variant (rs397507178) in RAD50 occurring in both ethnic groups. Again, 17 African and 20 European pathogenic variants appear to be unique between the ancestries, suggesting the contribution of inherited variance in genes responsible for telomere maintenance as contributors to PCa ancestral disparities.