The conserved transcription factor HSF-1 is essential to cellular stress resistance and organismal lifespan determination. The canonical function of HSF-1 is to regulate a network of molecular chaperones that maintain protein homeostasis during extrinsic environmental stresses or intrinsic age related deterioration. In the metazoan C. elegans, we engineered a modified HSF-1 strain that increases stress resistance and longevity without enhancing chaperone induction. This HSF-1 dependent health assurance acts through the regulation of pat-10. Upon heat stress pat-10 upregulation maintains a functional actin cytoskeleton and endocytic network. Loss of pat-10 causes a collapse of organismal health and failure of stress resistance. Furthermore, overexpression of pat-10 is sufficient to increase both thermotolerance and longevity by mechanisms that affect actin stability. Our findings indicate that in addition to chaperone induction, HSF-1 plays a prominent role in cytoskeletal integrity to ensure proper cellular function during times of stress and aging.