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Trypanosomes belonging to <i>Trypanosoma theileri</i> group are mammalian blood parasites with keds and horse fly vectors. Our aim is to study to vector specificity of <i>T. theileri</i> trypanosomes. During our bloodsucking Diptera survey, we found a surprisingly high prevalence of <i>T. theileri</i> trypanosomes in mosquitoes (154/4051). Using PCR and gut dissections, we detected trypanosomes of <i>T. theileri</i> group mainly in <i>Aedes</i> mosquitoes, with the highest prevalence in <i>Ae. excrucians</i> (22%), <i>Ae. punctor</i> (21%), and <i>Ae. cantans/annulipes</i> (10%). Moreover, <i>T. theileri</i> group were found in keds and blackflies, which were reported as potential vectors for the first time. The vectorial capacity was confirmed by experimental infections of <i>Ae. aegypti</i> using our isolates from mosquitoes; sand fly <i>Phlebotomus perniciosus</i> supported the development of trypanosomes as well. Infection rates were high in both vectors (47–91% in mosquitoes, 65% in sandflies). Furthermore, metacyclic stages of <i>T. theileri</i> trypanosomes were observed in the gut of infected vectors; these putative infectious forms were found in the urine of <i>Ae. aegypti</i> after a second bloodmeal. On the contrary, <i>Culex pipiens quinquefasciatus</i> was refractory to experimental infections. According to a phylogenetic analysis of the 18S rRNA gene, our trypanosomes belong into three lineages, TthI, ThII, and a lineage referred to as here a putative lineage TthIII. The TthI lineage is transmitted by Brachycera, while TthII and ThIII include trypanosomes from Nematocera. In conclusion, we show that <i>T. theileri</i> trypanosomes have a wide range of potential dipteran vectors, and mosquitoes and, possibly, sandflies serve as important vectors.