Vector-borne pathogens exist in obligate transmission cycles between vector and reservoir host species. Host shifts can lead to geographic expansion and the emergence of new diseases. Three etiological agents of human Lyme borreliosis (Borrelia afzelii, Borrelia bavariensis, and Borrelia garinii) predominantly utilize two distinct tick species as vectors in Asia (Ixodes persulcatus) and Europe (Ixodes ricinus) but how and in which order they colonized each continent remains unknown. Here, by reconstructing the evolutionary history of 142 Eurasian isolates, we show that all three Borrelia genospecies evolved from an Asian origin, suggesting that successful expansion into Europe resulted through invading a novel vector. The pattern of gene flow between continents is different between genospecies and most likely conditioned by reservoir host association and their dispersal. Our results highlight that Eurasian Lyme borreliosis agents are all capable of geographic expansion through vector shifts, but potentially differ in their capacity as emergent pathogens.