Previously either regarded as insignificant or feared as potential sources of infection, the bacteria living on our skin are increasingly recognized for their role in benefitting human health. Skin commensals modulate mucosal immune defenses and directly interfere with pathogens; however, their contribution to the skin’s physical integrity is less understood. Here, we show that the abundant skin commensal Staphylococcus epidermidis contributes to skin barrier integrity. S. epidermidis secretes a sphingomyelinase that acquires essential nutrients for the bacteria and assists the host in producing ceramides, the main constituent of the epithelial barrier that averts skin dehydration and aging. In mouse models, S. epidermidis significantly increases skin ceramide levels and prevents water loss of damaged skin in a fashion entirely dependent on its sphingomyelinase. Our findings reveal a symbiotic mechanism that demonstrates an important role of the skin microbiota in the maintenance of the skin’s protective barrier. Display omitted •Commensal Staphylococcus epidermidis contributes to skin barrier homeostasis•S. epidermidis produces a sphingomyelinase that helps generate protective ceramides•Sphingomyelinase contributes to S. epidermidis skin colonization•S. epidermidis prevents skin dehydration via its sphingomyelinase activity Ceramides are a key constituent of the skin barrier that prevent skin dehydration and aging. Zheng et al. show that the abundant skin commensal Staphylococcus epidermidis secretes a sphingomyelinase that facilitates host production of ceramides to help maintain skin integrity and prevent water loss of damaged skin.