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Cells induce conserved defense mechanisms that protect them from oxidative stress. How these defenses are regulated in multicellular organisms is incompletely understood. Here, we show that the heat shock transcription factor HSF-1 protects the nematode Caenorhabditis elegans from the oxidative stress caused by environmental peroxide. In response to a heat shock or a mild temperature increase, HSF-1 protects the nematodes from subsequent peroxide stress in a manner that depends on HSF-1’s transactivation domain. At constant temperature, HSF-1 protects the nematodes from peroxide stress independently of its transactivation domain, likely by inducing the expression of asp-4/cathepsin and dapk-1/dapk. Thus, two distinct HSF-1-dependent processes protect C. elegans from peroxide stress.