Tumor-associated macrophages (TAMs) are profoundly shaped by metabolic cues within the tumor microenvironment (TME). However, how amino acid metabolism determines TAMs fate remains poorly understood. Here, we identified methionine as a dominant regulator of macrophage anti-tumor immunity. Using methionine restriction diets in tumor-bearing mice, we show that limiting methionine availability reprograms macrophages toward an M1-like, anti-tumor state that restrains tumor progression. Mechanistically, reduced methionine metabolism suppressed macrophage hydrogen sulfide (H2S) production, thereby limiting a previously unrecognized S-sulfhydration of acetyl-CoA acetyltransferase 1 (ACAT1). Loss of ACAT1 sulfhydration impairs lipid metabolism and reprograms TAMs from an M2-like pro-tumor state to an M1-like anti-tumor phenotype. Conversely, restoration of H2S signaling or ACAT1 activity reverses methionine restriction-induced anti-tumor function and re-establishes a pro-tumorigenic phenotype. Notably, inhibition of ACAT1 in vivo recapitulates the anti-tumor effects of methionine restriction and synergizes with PD-1 blockade therapy. Clinically, reduced methionine pathway activity or lower ACAT1 expression in human cancers correlates with improved prognosis. These findings identify a diet-responsive immunometabolic pathway through an H2S-ACAT1 axis that governs TAMs fate, highlighting a metabolically driven strategy to reprogram the TME and enhance immunotherapy efficacy.