Specialized endoplasmic reticulum (ER) bodies in Brassicaceae plants facilitate defense against herbivores by storing β-glucosidases that activate toxic compounds upon tissue damage. The mechanisms ensuring the structural integrity and enzymatic activities of the ER body are unknown. In this study, we investigated the role of the mid-SUN-POD1 complex in ER-body function. Using Arabidopsis thaliana sun3 sun4 sun5 triple mutants and POLLEN DEFECTIVE IN GUIDANCE1 (POD1)-knockdown lines, we examined ER-body morphology through confocal microscopy, assessed glucosinolate degradation via LC-MS, and evaluated herbivore resistance through woodlice (Armadillidium vulgare) feeding assays. Both sun3 sun4 sun5 and POD1-knockdown plants exhibited fragmented ER bodies, constitutive ER stress, and increased susceptibility to herbivores, despite normal accumulation of ER-body proteins. The defects in ER-body morphology directly impaired the defense function of these structures rather than affecting protein abundance. The mid-SUN-POD1 complex is critical for ER-body morphogenesis and antiherbivore defense in Arabidopsis. Our findings demonstrate how this conserved ER membrane regulatory system contributes to the function of specialized ER-derived organelles and their role in plant defense.