This study contributes ancient mtDNA data to the research on Hungarian ethnogenesis and the conquest-period. We present the first described Avar-period ancient DNA dataset (n = 31), an almost four-fold enlargement of the existing Hungarian conquest-period dataset (with n = 76), and a magnified dataset from the Hungarian-Slavic contact zone of the 10–12th centuries (with n = 4). These together with the previously published 10th–12th century results were compared with published ancient and modern Eurasian mtDNA data. The results comprehensively demonstrate the conqueror maternal gene pool as a mixture of West Eurasian and Central/North Eurasian elements. Both the linguistically recorded Finno-Ugric roots and the Turkic, Central Asian influxes had possible genetic imprints in the conquerors’ mixed genetic composition. The small number of potential intra-site maternal relations compared to the number of detected inter-sites relations suggests that conqueror communities were mobile within the Carpathian Basin. Our data support the complex series of population genetic events before and during the formation of the 10th-century population of the Carpathian Basin. These processes might be defined by future ancient DNA studies focusing in the Ural region and in the Eastern European steppe using genome-wide sequencing techniques.