Resident tissue macrophages (RTMs) integrate local and systemic signals to coordinate immune cell function at homeostasis and in response to inflammatory stimuli. Obesity-associated metabolic dysfunction drives the development of RTM populations that contribute to disease states in multiple tissues. However, the contribution of specific dietary components to innate immune cell activation and function, as opposed to the effects of obesity per se, is largely unknown. Herein, we used 1) novel diets supplemented with single lipids, 2) mice lacking components of the NLRP3 inflammasome, or treated with pharmacologic inhibitors of IRE1⍺, and 3) models of neutrophilic asthma and pulmonary viral infection to characterize the mechanisms by which high fat (HF) diets shape lung RTM phenotype and function in the steady state and influence responses to inflammatory insults. We report that during HF diet feeding lung RTMs accumulate saturated long chain fatty acids (LCFA), specifically stearic acid (SA), and demonstrate features of NLRP3 inflammasome priming and activation. In vitro, SA-induced macrophage inflammasome priming was dependent on de novo phosphatidylcholine synthesis and IRE1⍺ endonuclease activity. In vivo, increased dietary SA caused IRE1⍺-dependent and RTM inflammasome-dependent lung inflammation in the steady state and exacerbated a model of innate airway inflammation, but protected against infection with SARS-CoV-2 infection. Conversely, increased dietary oleic acid, the monounsaturated counterpart of SA, reduced inflammasome activation in the steady state and attenuated neutrophilic airway inflammation. Importantly, we identified a population of lung monocytes with hallmarks of HF diet-induced RTM activation that are present in obese humans with asthma. Together, these results identify a class of dietary lipids that regulate lung RTM phenotype and function in the steady state and modulate the severity of inflammation in the lung.