G protein‐coupled receptors (GPCRs) are the largest superfamily of cell surface receptors. They regulate critical physiological events and serve as potential therapeutic targets. G protein‐coupled receptor 35 (GPR35), a class A rhodopsin‐like GPCR expressed in various tissues, including adipose tissue and the gastrointestinal tract, has roles in diverse functions, including antioxidant, anticarcinogenic, and anti‐inflammatory effects. Although many endogenous and synthetic GPR35 agonists have been identified, the understanding of food‐derived agonists is limited. In this study, we discovered pelargonidin as a newly identified food‐derived GPR35 agonist through a systematic screening approach. We evaluated 28 dietary phytochemicals using a transforming growth factor α (TGFα) shedding assay to evaluate GPR35 activation, and found that cyanidin, a common 3‐hydroxyanthocyanidin present in various red fruits and vegetables, induced GPR35 activation. Among a series of 3‐hydroxyanthocyanidins tested, pelargonidin, characterized by its monohydroxylated B‐ring, exhibited the most potent agonistic activity. Mutational studies demonstrated that the hydrogen bond between the 3‐hydroxy group in the C‐ring of pelargonidin and Asn169, as well as the hydrophobic interaction between the A‐ring of pelargonidin and Phe163, is crucial for GPR35 activation. Furthermore, pelargonidin inhibited the production of interleukin‐8, a pro‐inflammatory cytokine, by activating endogenous GPR35 in Caco‐2 cells. These findings suggest that GPR35 may serve as a potential receptor for dietary anthocyanidins, such as pelargonidin, and provide new insights into the molecular mechanisms underlying the potential chemopreventive effects of anthocyanidins.