Tissue-resident macrophage populations are maintained or expanded by local proliferation and, in nematode infection, this requires interleukin-4 (IL-4). This study shows that the expression of IL-4 receptor-α (IL-4Rα) by macrophages confers a competitive advantage, allowing higher and more sustained proliferation of IL-4Rα+ compared with IL-4Rα− resident macrophages. Early during nematode infection, proliferation is IL-4Rα independent and is controlled by colony-stimulating factor 1 (CSF1). As the immune response progresses, proliferation and alternative activation become dependent on IL-4. The authors suggest that the IL-4 pathway allows the outgrowth of resident macrophages when CSF1 is limiting without a coincident increase in monocyte recruitment.