Tissue-resident macrophages represent a highly heterogeneous population which integrates the ontogenic information with tissue-specific and niche-specific cues to carry out their assigned functions and maintain tissue homeostasis. The proclivity of tissue-resident macrophages to maintain tissue homeostasis is exploited by tumours to their own benefit. One of the highly specialised macrophage subsets known as perivascular macrophages have been shown to promote pro-tumoural activities at the primary as well as metastatic sites. At the site of primary tumour, they have been implicated in aiding tumour cell intravasation, promoting angiogenesis and promoting tumour relapse after therapy. At the metastatic site, they have been implicated in aiding tumour cell extravasation and maintaining tumour cell dormancy. However, how perivascular macrophages develop within tumours has remained unclear. It is now well appreciated that most tissue-resident macrophages develop from consecutive waves of CD115(CSF1-R)+ precursor populations during embryonic development. However, in adults, HSC-derived monocytes represent the sole source for the generation of macrophages within inflamed tissues. We have now identified novel progenitor cells residing within the adult bone marrow that are capable of efficiently generating macrophages at inflammatory sites and within tumours. These novel precursors were solely responsible for the replenishment of pro-tumoural perivascular macrophages, as monocytes and their precursors failed to give rise to these cells. Finally, we found these precursors to exist within the developing embryo prior to the emergence of tissue-resident macrophages as well as HSCs reiterating that they may represent a separate progenitor from classical defined EMPs or fetal liver monocytes within the embryo. Together, our data challenges a central tenet of haematopoiesis which advocates for an obligatory relationship between monocytes and macrophages under inflammation and during tumour development. Furthermore, our data highlights a hitherto undescribed pathway of macrophage generation in adults in the setting of inflammation and tumour development.