Macrophage (MØ) biology is routinely modelled in the peritoneal cavity, a vascular tissue readily infiltrated by leukocytes during inflammation. After several decades of study, no consensus has emerged regarding the importance of in situ proliferation versus peripheral monocyte recruitment for the maintenance of tissue resident MØs. By applying specific measures of mitosis, we have monitored tissue MØ proliferation during newborn development, adulthood and acute resolving inflammation in young adult mice. Despite the vascular nature of the tissue and ease of peripheral leukocyte entry, tissue MØs in the newborn increase in number by local proliferation. On the contrary, in the adult, tissue MØ proliferation is considerably reduced and most likely provides homeostatic control of cell numbers. Importantly, during an acute inflammatory response, when substantial numbers of inflammatory MØs are recruited from the circulation, tissue‐resident MØs survive and then undergo a transient and intense proliferative burst in situ to repopulate the tissue. Our data indicate that local proliferation is a general mechanism for the self‐sufficient renewal of tissue MØs during development and acute inflammation and not one restricted to non‐vascular tissues, which has implications for the therapeutic modulation of MØ activity during the resolution of inflammation.