Adipocytes and hepatocytes are both capable of lipid storage; however, the determinants that govern lipid partitioning between these cell types remain unclear. In mice subjected to high-fat diet feeding, lipid accumulation occurs predominantly in adipocytes during the early phase, whereas hepatic steatosis emerges mainly after epididymal adipocyte death, which elevates circulating free fatty acids and promotes lipid deposition in hepatocytes. Nonetheless, it is uncertain whether additional signals derived from adipocyte death are required to direct lipid storage in hepatocytes and initiate metabolic dysfunction–associated steatotic liver disease (MASLD, previously termed nonalcoholic fatty liver disease). By employing genetically engineered mouse models in conjunction with bulk and single-cell RNA sequencing, we identified that visceral adipocyte death provokes the hepatic accumulation of S100A8⁺ macrophages, a process partially driven by free fatty acids and apoptotic adipocyte–derived extracellular vesicles. Deletion of S100a8 specifically in macrophages attenuated hepatic lipid accumulation and mitigated MASLD severity. Mechanistically, S100A8⁺ macrophages suppressed cellular communication network factor 3 (CCN3), a negative regulator of CD36, thereby augmenting CD36 expression in hepatocytes. Collectively, these findings indicate that adipocyte death promotes hepatic infiltration of S100A8⁺ macrophages, which facilitate hepatocyte lipid storage and accelerate MASLD progression through CD36 upregulation, in part via suppression of CCN3.