Proteasome dysfunction can lead to an autoinflammatory disease associated with elevated type I interferon (IFNαβ) and NF-κB signalling, however the innate immune pathway driving this inflammation is currently unknown. Here, we identify Protein Kinase R (PKR) as an innate immune sensor for proteotoxic stress. PKR activation was observed in cellular models of decreased proteasome function and in cells from proteasome-associated autoinflammatory disease (PRAAS) patients. Furthermore, genetic deletion or small molecule inhibition of PKR ameliorated inflammation in these contexts. PKR is a rheostat for proteotoxic stress, its activation triggers phosphorylation of eIF2α which prevents the translation of new proteins, thereby promoting a cell’s return to homeostasis. Although traditionally known as a sensor of RNA, under conditions of proteasome dysfunction PKR senses the cytoplasmic accumulation of a known interactor, interleukin 24 (IL-24). Importantly, blocking misfolded IL-24 egress into the cytosol via the endoplasmic reticulum degradation pathway blunted PKR activation and subsequent inflammatory signalling. Cytokines such as IL-24 are normally secreted, therefore cytoplasmic accumulation of IL-24 represents a danger associated molecular pattern for the cell. Thus, we have identified a novel mechanism by which cells sense proteotoxic stress, causing inflammation observed in the disease PRAAS.