Lung cancer is initiated by stochastic processes that depend on competition between mutant and normal adult stem cells. The mesenchymal niche responsible for cancer initiation is unknown. We generated alveolar type 2 (AT2)-specific Pten-deficient (AT2-PtenKO) mice and analyzed the characteristics of the alveolar mesenchyme by a single-cell RNA-seq analysis. Over 70% of the AT2-PtenKO mice spontaneously developed lung adenocarcinoma at 1 year old. The population RNA-seq of isolated AT2 and mesenchymal cells from 16-week-old age AT2-PtenKO mice showed increased receptor-ligand activity in AT2 and upregulated immune-response activation signaling in mesenchymal cells, respectively. The single-cell RNA-seq identified the emergence of a rare mesenchymal subpopulation in 16-week-old AT2-PtenKO mice. Violin plots showed that this subpopulation expressed a group of components of mitochondrial NADH dehydrogenase complex I (MT-NDs) at high levels across the board. By using hashtag demultiplexing, we observed a 5.5-fold increase in the MT-NDs-expressing subpopulation in AT2-PtenKO mice compared to controls (p=0.0286). AT2-specific ablation of Pten accelerated cellular senescence in AT2 cells from a young age. In an unaffected old age stage, AT2-PtenKO mice showed spontaneous inflammatory cell recruitment in lung parenchyma. Our results suggest that AT2-Pten deficiency accelerates AT2 cellular senescence, perturbs the mesenchymal subpopulation's distribution, induces the emergence of an MT-NDs-expressing mesenchymal subpoplulation, and creates hyper-immunoreactivity in the alveolar microenvironment, resulting in a disruption of AT2-mesenchymal cell crosstalk and lung tumorigenesis.