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The Janus kinase/signal transducers and activators of transcription (JAK/STAT) signaling pathway play a pivotal role in innate immunity. Among invertebrates, Domeless receptors serve as the key upstream regulators of this pathway. In our study on Bactrocera dorsalis, we identified three cytokine receptors: BdDomeless1, BdDomeless2, and BdDomeless3. Each receptor encompasses five fibronectin-type-III-like (FN III) extracellular domains and a transmembrane domain. Furthermore, these receptors exhibit the increased responsiveness to diverse pathogenic challenges. Notably, only BdDomeless3 is upregulated during symbiont-like viral infections. Moreover, silencing BdDomeless3 enhanced the infectivity of Bactrocera dorsalis cripavirus (BdCV) and B. dorsalis picorna-like virus (BdPLV), underscoring BdDomeless3’s crucial role in antiviral defense of B. dorsalis. Following the suppression of Domeless3 expression, six antimicrobial peptide genes displayed decreased expression, potentially correlating with the rise in viral infectivity. To our knowledge, this is the first study identifying cytokine receptors associated with the JAK/STAT pathway in tephritid flies, shedding light on the immune mechanisms of B. dorsalis.