Synovial joints harbour a protective lining layer that consists of macrophages and fibroblasts. is disrupted in inflamed joints. It is currently unclear exactly when lining macrophages are established during development, and from which progenitor sources. Here, we delineated the development of synovial lining macrophages using a combination of genetic models, confocal imaging and single-cell transcriptomics. We report that the synovial lining is immature at birth and is established within the first three weeks of life. Lining macrophages develop and maintain themselves with minimal monocyte contribution. Instead, the lining gradually incorporates pre-existing foetal-derived macrophages, which acquire the characteristic transcriptional identity of the lining population. Lining macrophage development critically depends on CSF1 signalling and further integrates e.g. TGFb signalling. This work provides a detailed understanding of how lining macrophages develop and forms the basis of addressing how they may be changed by adverse environments in early life, which are increasingly recognised as contributing factors to susceptibility to immune-mediated pathology, including arthritis.