Rickettsia
species, which constitute obligate intracellular bacteria adapted to a host-dependent lifestyle, have traditionally been classified into four phylogenetic groups. However, the available genomes are biased toward the Typhus and Spotted Fever groups, with early-diverging Ancestral group (AG) lineages being underrepresented. Here, we isolated six
Candidatus
Rickettsia mendelii strains from
Ixodes turdus
ticks in Japan. We obtained their whole-genome sequences, including one closed genome, and found that they form a distinct lineage in the AG and have the smallest genome among the known rickettsial species. Gene tree-aware reconstruction of evolutionary events using amalgamated likelihood estimation revealed that the last common ancestor of
Rickettsia
had a smaller gene family size than modern species do, and
Ca
. R. mendelii retains the most similar genomic content to this ancestral state. Various patterns of gene gain and loss among
Rickettsia
lineages were also suggested, highlighting their divergent evolutionary trajectories. These findings increase our understanding of
Rickettsia
genome evolution.