The Y chromosome (chrY) is notoriously difficult to investigate due to its highly repetitive nature and has often been ignored in many genomic investigations into associations with disease. Prostate cancer (PCa) is a highly heritable cancer with significant ethnic disparity, with African men at greatest risk of mortality, and little has been done to investigate the contribution of the Y chromosome to this disparity. Here, using a unique multi-ethnic PCa resource (106 African, 57 European), comprised of whole genome sequences from the blood and tumour, and multi-informatic methods of interrogation, we tackle the poorly chartered genomic landscape of chrY. While African men presented with significantly higher number of germline variance representing earliest diverged paternal human haplogroups, conversely within chrY genetic diversity was greatest for men of European ancestry representing recent divergence. Potentially deleterious germline variants were found in both European (one in TBL1Y, three in USP9Y) and African patients (one in UTY and one in KDM5D) that could contribute to PCa susceptibility. Somatic copy number alterations were more common in HRPCa patients, and present in more genes in African tumours (166 RNA and protein-coding genes) than European tumours (58 genes). However, shared alterations between ethnicities were noted in DDX3Y and USP9Y, while losses in KDM5D, PCDH11Y and RBMY genes were more prevalent in African tumours. Overall, we report the inherited and acquired variation in the chrY landscape between ethnicities. The differences in somatic copy number alterations between African and European tumours point towards pathways for treatment-resistant tumours in African patients, a possible contributor to the worsened PCa mortality rates for African men. As there were a greater number of genes altered in African tumours, further work is needed to explore epigenetic and expression differences for how this variation may affect tumour progression.