Disrupting sleep during development leads to lasting deficits in chordates and arthropods. To address lasting impacts of sleep deprivation in C. elegans, we established a nonlethal deprivation protocol. Deprivation triggered protective insulin-like signaling and two unfolded protein responses (UPRs): the mitochondrial (UPRmt) and the endoplasmic reticulum (UPRER) responses. While the latter is known to be triggered by sleep deprivation in rodent and insect brains, the former was not strongly associated with sleep deprivation previously. We show that deprivation results in a feeding defect when the UPRmt is deficient. In contrast, deprivation causes germ cell apoptosis and excess twitching in vulval muscles when the UPRER is deficient, mirroring a trend caused by loss of egg-laying command neurons. These data show that nonlethal deprivation of *C. elegans* sleep causes proteotoxic stress. Unless mitigated, distinct types of deprivation-induced proteotoxicity can lead to anatomically and genetically separable lasting defects. The relative importance of different UPRs post-deprivation likely reflects functional, developmental, and genetic differences between the respective tissues and circuits.