Rubella virus (RuV) causes rubella and, through maternal infection during pregnancy, congenital rubella syndrome (CRS). Despite its clinical significance, the cellular entry mechanism of RuV remains poorly understood due to limited identification of host receptors, impeding pathogenesis research and therapeutic development. Here we show that Nectin-4 acts as the primary RuV cellular receptor using proximity biotin labeling-based proteomics and CRISPR/Cas9 screening. This receptor is shared with measles virus, indicating convergent evolution in viral entry. Nectin-4 directly binds RuV via its ectodomain, mediating calcium-independent viral attachment and endocytic internalization. In respiratory epithelial cells, Nectin-4 enables basolateral RuV entry with apical progeny release. Using human placental organoid models, we identified syncytiotrophoblasts as initial RuV infection targets, with infection significantly reduced upon Nectin-4 inhibition. These findings establish Nectin-4 as critical for both respiratory transmission and maternal-fetal vertical transmission of RuV. Our results provide key insights into RuV pathogenesis and identify Nectin-4 as a potential therapeutic target for CRS prevention. Importantly, the shared receptor usage with measles virus enables integrated approaches for eliminating both rubella and measles.