Several bacterial pathogens have transitioned from tick-borne to louse-borne transmission, which often involves genome reduction and increasing virulence. However, the timing of such transitions remains unclear. We sequenced four ancient Borrelia recurrentis genomes, the agent of louse-borne relapsing fever, dating from 2300 to 600 years ago. We estimated the divergence from its closest tick-borne relative to 6000 to 4000 years ago, which suggests an emergence coinciding with human lifestyle changes such as the advent of wool-based textiles. Pan-genome analysis indicated that much of the evolution characteristic of B. recurrentis had occurred by ~2300 years ago, though further gene turnover, particularly in plasmid partitioning, persisted until ~1000 years ago. Our findings provide a direct genomic chronology of the evolution of this specialized vector-borne pathogen.