Sperm production is physiologically costly. Consequently, males are expected to be prudent in their sperm production, and tailor their expenditure according to prevailing social conditions. Differences in sperm production have been found across island populations of house mice that differ in the level of selection from sperm competition. Here, we determined the extent to which these differences represent phenotypic plasticity and/or population divergence in sperm production. We sourced individuals from two populations at the extreme levels of sperm competition, and raised them under common-garden conditions while manipulating the social experience of developing males. Males from the high-sperm competition population produced more sperm and better quality sperm than did males from the low-sperm competition population. In addition, males reared under a perceived “risk” of sperm competition produced greater numbers of sperm than males reared with “no risk.” However, our analyses revealed that phenotypic plasticity in sperm production was greater for individuals from the high-sperm competition population. Our results are thus consistent with both population divergence and phenotypic plasticity in sperm production, and suggest that population level of sperm competition might affect the degree of adaptive plasticity in sperm production in response to sperm competition risk.