Genome sequencing studies of families have revealed that ~30 to 100 point mutations are acquired spontaneously at each generation. These newly arising (de novo) mutations (DNMs) originate mostly from the paternal germline and increase in frequency with the father’s age. The full range of mechanisms that lead to the emergence of DNMs is not well understood. Traditionally, germline and somatic spontaneous mutations are usually considered to represent two distinct genetic entities, originating in different cell types and at different times in development. However, somatic mutations can also arise in the germline. These can be passed on to the next generation as DNMs but can also lead to cancer in rare cases. Using whole genome sequencing and novel bioinformatics approaches, we have explored the mechanisms leading to the occurrence of spermatocytic tumour (SpT), a rare testicular tumour that, when diagnosed in older men, is associated to the clonal expansion of mutations in the testis due to selection. We found that SpTs are characterised by recurrent whole-chromosome aneuploidies but they carry an extremely low mutation load of 0.2 SNVs/Mb. The mutational signature in SpT recapitulates the features of DNMs found by family studies. Our results indicate that evolutionary pressure must be imposed on the germline to maintain low mutation rate and ensure faithful transmission of genomic information generation after generation.