Mast cells are distributed at environmental interfaces including the skin where they play a critical role in immune responses to infection and in neutralizing venoms and toxins. Mast cells are also central mediators of allergy and have been implicated in the pathogenesis of inflammatory skin diseases such as atopic dermatitis. Despite their importance in health and disease, the mechanisms underlying mast cell homeostasis in the skin remain poorly understood. We have used multiphoton microscopy of mast cell reporter mice to characterise the dynamics of mast cell proliferation within the skin dur- ing skin homeostasis and following inflammation in vivo. We show that while skin mast cells are self-renewing and radioresistant during steady-state, mast cell repopulation following inflammation is mediated by bone marrow-derived progenitors. We further functionally characterise the mast cell progenitor population in vivo and provide new insight into the mechanisms underlying their recruitment to the skin. These findings have implications for our understanding of the pathogenesis of inflammatory skin dis- eases including atopic dermatitis and cutaneous mastocytosis.