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European bat lyssavirus 1 (EBLV‐1) is a widespread lyssavirus across Europe, whose epizootic cycle is linked to a few bat species. Occasionally, EBLV‐1 infection may occur in domestic animals and humans. EBLV‐1 can be classified into two subtypes, where subtype EBLV‐1a shows a wide geographic distribution between France and Russia whereas subtype EBLV‐1b is distributed between Spain and Poland. In this study, we determined the genome sequence of two recent EBLV‐1a strains detected in Hungary and analysed their adaptive evolution and phylodynamics. The data set that included 100 EBLV‐1 genome sequences identified positive selection at selected sites in genes coding for viral proteins (N, codon 18; P, 141 and 155; G, 244 and 488; L, 168, 980, 1597 and 1754). A major genetic clade containing EBLV‐1a isolates from Hungary, Slovakia, Denmark and Poland was estimated to have diverged during the 19th century whereas the divergence of the most recent ancestor of Hungarian and Slovakian isolates dates back to 1950 (time span, 1930 to 1970). Phylogeographic analysis of the EBLV‐1a genomic sequences demonstrated strong evidence of viral dispersal from Poland to Hungary. This new information indicates that additional migratory flyways may help the virus spread, a finding that supplements the general theory on a west‐to‐east dispersal of EBLV‐1a strains. Long‐distance migrant bats may mediate the dispersal of EBLV‐1 strains across Europe; however, structured surveillance and extended genome sequencing would be needed to better understand the epizootiology of EBLV‐1 infections in Europe. [ABSTRACT FROM AUTHOR]