<p>Dental pulp homeostasis and regeneration rely on specialized mesenchymal populations, yet aging promotes fibrotic remodeling and functional decline. Here, using the continuously growing mouse incisor as an experimentally tractable model, we integrate single-cell RNA sequencing, spatial transcriptomics, lineage tracing, and functional assays to investigate age-associated pulp remodeling. We identify a distinct <i>Lypd1</i>⁺ fibroblast progenitor population that is particularly vulnerable to age-associated dysfunction. Lineage tracing and trajectory analysis show that these cells originate from the <i>Sfrp2</i>^hi stem cell pool, while functional studies of MACS-isolated human LYPD1⁺ cells provide supportive evidence for a related progenitor-like state. Notably, early aging preferentially affects <i>Lypd1</i>⁺ progenitors, rather than <i>Sfrp2</i>^hi stem cells, promoting fibrotic conversion through aberrant upregulation of 11β-HSD2, which enhances aldosterone-mediated mineralocorticoid receptor (MR)-associated signals. Additionally, aging promotes the accumulation of <i>Ccl4</i>⁺ macrophages that establish a pro-inflammatory niche, where macrophage-derived PDGFB induces 11β-HSD2 via the P38 MAPK signaling. In vivo inhibition of the PDGF/P38/11β-HSD2 axis attenuates age-related pulp fibrosis. Together, our findings indicate that age-associated pulp fibrosis in this model is driven, at least in part, by niche-mediated metabolic reprogramming of progenitor cells rather than intrinsic stem cell exhaustion, highlighting corticosteroid metabolism as a potential therapeutic target for fibrotic degeneration in aging dental pulp.</p><p></p>