The responses of plants to auxin and phosphate (Pi) starvation are closely linked. However, the underlying mechanisms connecting the Pi starvation (-Pi) responses to auxin are largely unclear. Here, we show that OsPht1;8 (OsPT8), a phosphate transporter, functions in both the auxin and -Pi responses in rice (Oryza sativa L.) and tobacco (Nicotiana tabacum). The overexpression of OsPT8 (OsPT8-Oe) led to the loss of sensitivity to auxin and -Pi in adventitious roots, lateral roots, and root hairs in rice. The expression levels of OsPT8 and pOsPT8::GUS staining in roots, root-shoot junctions and leaves of rice were induced by IAA treatments. The number of young lateral roots in the OsPT8-Oe transgenic rice, which had higher auxin concentrations, was distinctly more than that in the wild-type, possibly as a result of increased expression of auxin-related genes under normal Pi condition. Moreover, tobacco overexpressing OsPT8 had a similar root phenotype to OsPT8-Oe rice. These data reveal a novel biological function of OsPT8 in the cross-talk between Pi and auxin signaling, and provide new evidence for the linkage between auxin and -Pi responses.