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Cells sense stress and initiate response pathways to maintain lipid and protein homeostasis. However, the interplay between these adaptive mechanisms is unclear. Herein, we demonstrate how imbalances in cytosolic protein homeostasis affect intracellular lipid surveillance. Independent of its ancient thermo-protective properties, the heat shock factor, HSF-1, modulates lipid metabolism and age regulation through the metazoan-specific nuclear hormone receptor, NHR-49. Reduced hsf-1 expression destabilizes the Caenorhabditis elegans enteric actin network, subsequently disrupting Rab GTPase-mediated trafficking and cell-surface residency of nutrient transporters. The ensuing malabsorption limits lipid availability, thereby activating the intracellular lipid surveillance response through vesicular release and nuclear translocation of NHR-49 to both increase nutrient absorption and restore lipid homeostasis. Overall, cooperation between these regulators of cytosolic protein homeostasis and lipid surveillance ensures metabolic health and age progression through actin integrity, endocytic recycling, and lipid sensing. [Display omitted] • Lipid deposition is modulated by HSF-1 levels in C. elegans • Lifespan extension by HSF-1 requires NHR-49 • Reduced hsf-1 expression impairs membrane trafficking through actin destabilization • Loss of hsf-1 activates the intracellular lipid surveillance response Watterson et al. describe a mechanism through which HSF-1 affects lipid homeostasis. Through its ability to stabilize the enteric actin network, HSF-1 promotes membrane trafficking, cellular absorption, and lipid accumulation. Loss of hsf-1 activates the intracellular lipid surveillance pathway via NHR-49, thereby linking cytosolic protein homeostasis with lipid metabolism. [ABSTRACT FROM AUTHOR]