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Cell surface translocation of endoplasmic reticulum (ER) chaperones, such as glucose\u2010regulated protein 78 (GRP78), during malignancy, drug resistance, and ER stress induced by therapies, offers a promising pan\u2010cancer target. To target GRP78, nanobody C5, identified from a phage library and exhibiting high affinity for human and mouse GRP78, is utilized to develop the <jats:italic>Pseudomonas<\/jats:italic> exotoxin (PE) immunotoxin C5\u2010PE38. C5\u2010PE38 induced ER stress, apoptosis and immunogenic cell death in targeted cells and showed antitumor efficacy against colorectal cancer and melanoma models without obvious toxicity. Mechanistically, transcriptome profiling showed that C5\u2010PE38 reshaped the tumor immune microenvironment with enhanced innate and adaptive immune response and response to interferon beta. 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