Stem and progenitor cells as well as the surrounding niche function in a coordinated and dynamic manner to promote tissue regeneration. The crosstalk between these cells within the lung is often highly complex. Recent efforts have helped simplify such complexity, especially through the use of genetic lineage tracing and single-cell RNA sequencing (scRNA-seq). We have previously identified a novel cell population that we termed ?repair-supportive mesenchymal cells? (RSMC), which is distinct from airway smooth muscle cells (ASMC) and is critical for regeneration of the conducting airway epithelium by secreting fibroblast growth factor 10 (FGF10). Those data were obtained by analyzing the ACTA2+ lineage that intersected with the glioma-associated oncogene 1-positive (GLI1+) lineage during the repair process. In order to better define this mesenchymal population, we decided to lineage-trace FGF10+ cells in the context of airway regeneration. Here, we used the novel Fgf10Cre-ERT2 line to label FGF10+ cells before and after naphthalene injury. To identify the RSMC cluster within the FGF10+ pool, we used scRNA-seq coupled to spatial mapping of lineage-labeled cells. Additionally, organoid assays were utilized to evaluate the ability of FGF10+ subsets to support club cell growth ex vivo. Our data provide cellular and spatial evidence for the contribution of FGF10+ cells to the RSMC population emerging after naphthalene injury. We uncover the genetic signature of the RSMC cluster and the possible involvement of WNT and Hippo signaling in the activation and migration of these cells. Future work aims to identify human counterparts in donor and COPD lung material.