Earth's rising temperature has substantial repercussions for food-producing animals by increasing morbidity and mortality, diminishing reproductive potential, and reducing productivity. In the dairy industry this equates to massive losses in milk yield, which occur when cows are exposed to heat stress during lactation or during the non-lactating period between lactations (i.e. dry period). Furthermore, milk yield is significantly lower in first-lactation heifers that experienced fetal heat stress. The mechanisms underlying intrauterine effects of heat stress on the offspring's future lactation have yet to be fully elucidated. We hypothesize that heat stress experienced through the intrauterine environment will alter the mammary gland microstructure and cellular processes involved in cell turnover during the cow's first lactation. Mammary biopsies were collected from first-lactation heifers that were exposed to heat stress or cooling conditions while developing in utero (IUHT and IUCL; respectively, n = 9-10). IUHT heifers produced less milk compared to IUCL. The mammary glands of IUHT heifers differed morphologically from IUCL, with the IUHT heifers having smaller alveoli and a greater proportion of connective tissue relative to their IUCL herdmates. However, intrauterine heat stress had little impact on the proliferation and apoptosis of mammary cells during lactation. Our results indicate that fetal exposure to heat stress impairs milk production in the first lactation, in part, by inducing aberrant mammary morphology. This may result from alterations in the developmental trajectory of the fetal mammary gland that persist through the first lactation rather than to alterations in the cellular processes controlling mammary cell turnover during lactation.