Aging nephropathy is characterized by podocyte depletion, accompanied by progressive glomerulosclerosis. Replacement of terminally differentiated podocytes by local stem/progenitor cells is likely a critical mechanism for their regeneration. Recent studies have shown that cells of renin lineage (CoRL), normally restricted to the kidney's extra-glomerular compartment, might serve this role following an abrupt depletion in podocyte number. To determine the effects of aging on the CoRL reserve, and if CoRL moved from an extra- to the intra- glomerular compartment during aging, genetic cell fate mapping was performed in aging Ren1cCre x Rs-ZsGreen reporter mice. Podocyte number decreased, and glomerular scarring increased with advanced age. CoRL number decreased in the juxta-glomerular compartment with age. There was a paradoxical increase in CoRL in the intra-glomerular compartment at 52 and 64 weeks of age, where a subset co-expressed the podocyte proteins nephrin, podocin and synaptopodin. Transmission EM studies showed that a subset of labeled CoRL in the glomerulus displayed foot processes, which attached to the GBM. No CoRL in the glomerular compartment stained for renin. These results suggest that despite a decrease in the reserve, a subpopulation of CoRL move to the glomerulus following chronic podocyte depletion in aging nephropathy, where they acquire a podocyte-like phenotype. This suggests that they might serve as adult podocyte stem/progenitors cells under these conditions, albeit in insufficient numbers to fully replace podocytes depleted with age.