Tembusu virus (TMUV) is a positive-sense RNA virus that is associated with severe reduction in egg production and even death in ducks. TMUV infection shows high incidence and is a threat to the global duck industry. However, the possible origin, genotype, and codon usage bias of TMUV are not very clear. Here, we addressed these questions by analyzing the available genomic sequences from China. The results showed that the ancestor of avian TMUV was most likely a mosquito TMUV. Moreover, three TMUV clades were identified by three different phylogenetic analysis methods. The TMUV genome exhibits a stronger mutation pressure than natural selection pressure. TMUV has the potential to cause an infection outbreak among humans, thereby posing a major threat to public health. Our findings provide important insights that reveal the ongoing TMUV spread in China and can aid in future prevention and control.