Abstract Diapause is a programmed developmental arrest process in insects. Diapause can occur at various stages of insect development and is frequently restricted to a specific developmental stage within a single species. In Bombyx mori , embryonic diapause is elicited by the diapause hormone (DH) and DH receptor (DHR) in diapause strains. Nevertheless, the regulatory mechanism through which BmDHR functions as a G protein‐coupled receptor (GPCR), to exert other physiological functions in nondiapause silkworms, remains unclear. In this study, we found that BmDHR had 7 alternative splice isoforms. A knockout experiment confirmed that BmDHR mediated the transduction of diapause signals. Interestingly, the loss of BmDHR caused partial precocious metamorphosis and an embryo‐lethal phenotype in nondiapause silkworms. An assessment of global transcriptional patterns revealed that BmDHR knockout affected physiological responses induced by manifold cellular processes, including the Toll/immune deficiency (Imd), Wnt, insulin‐like growth factor, Hedgehog and P38/mitogen‐activated protein kinase (MAPK) signaling pathways. This study expands our knowledge of the physiological roles for DHR in insect growth and development.