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Cowpea mild mottle virus (CPMMV, genus Carlavirus, family Betaflexividae) is an economically important virus infecting soybeans in Brazil, where it was initially identified in 1983. CPMMV is transmitted by the whitefly, Bemisia tabaci, and occasionally by seeds. Over the last three decades, the most invasive B. tabaci Middle East–Asia Minor 1 (MEAM1), and lately the Mediterranean (MED) cryptic species, have replaced the indigenous species in Brazil, with MEAM1 being predominant. In this study, we investigated the transmission properties of CPMMV by MEAM1 and MED, and their distribution in major soybean-growing areas in São Paulo State. Our results from transmission assays with a single insect revealed that MED is a more efficient vector compared to MEAM1, transmitting the virus within a two-minute inoculation access period. B. tabaci MEAM1 is still the predominant whitefly species in São Paulo State, but MED was also identified in different places, mainly in mixed infestations with MEAM1. Some areas transitioned to a predominance of MED over the three years, while others, where MED had previously been detected, showed a reduction in the insects during the same period. Understanding the transmission dynamics of CPMMV and the distribution of its vectors is crucial for implementing effective management strategies to control the virus spread and protect soybean crops. Further research into the mechanisms driving the shifts in whitefly species dominance and CPMMV distribution will be essential for sustaining soybean production in Brazil.