Disruptions to autophagy, mitochondrial biology, and glycolysis are recognized features of alveolar type 2 (AT2) cell stress associated with human IPF. We aimed to leverage our published inducible murine Sftpc^I73T (I^ER-SP-C^I73T) model of lung fibrosis to catalogue AT2 metabolic dysfunction, identify therapeutic targets, and gauge effect size from focused rescue of the disease phenotype. Primary Sftpc^I73T AT2 cells (AT2^I73T) exhibit acquired autophagic defects that coincide with transcriptomic upregulation in glucose utilization / carbohydrate metabolism pathways and functional biochemical increases in glucose flux and extracellular lactate. In ?Seahorse? assays, AT2^I73T isolated 2- and 4-weeks post-induction show progressive impairment in respiration along with decreased (depolarized) mitochondrial transmembrane potential (??), disruption of mitochondrial networks (increased fission), and a concurrent decrease in mitochondrial biogenesis. AT2^I73T bioenergetic changes were associated with increased AT2 cellular ATP content and inhibition of the AMPK-PPAR? signaling hub. In primary AT2^I73T, AMPK agonism (PF06409577) or stimulation of PGC1? (Rosiglitazone), but not mTOR inhibition (Rapamycin) rescued mitochondrial respiration. In vivo proof of concept was done using Metformin (indirect AMPK agonist) in preventative or therapeutic protocols. Delivered once daily to Sftpc^I73T mice, Metformin reduced mortality, BAL protein, and BAL soluble collagen while improving static lung compliance. Together the data support a role for epithelial metabolic dysfunction in IPF mediated by AT2 glycolytic reprogramming, mitochondrial dysfunction, and altered AMPK signals.