The family Anaplasmataceae includes tick-borne bacteria of major public and veterinary health interest, as best illustrated by members of the generaAnaplasmaandEhrlichia. Recent epidemiological surveys have also reported on the presence of a novel putative genus in the Anaplasmataceae,CandidatusAllocryptoplasma, previously described asCandidatusCryptoplasma in the western black-legged tick,Ixodes pacificus. However, the genetic diversity ofCa.Allocryptoplasma and its phylogenetic relationship with other Anaplasmataceae remain unclear. In this study, we developed a multi-locus sequence typing approach, examining the DNA sequence variation at five genes ofCa.Allocryptoplasma found in ticks. Combining this multi-locus sequence typing and genetic data available on public databases, we found that substantial genetic diversity ofCa.Allocryptoplasma is present inIxodes,AmblyommaandHaemaphysalisspp. ticks on most continents. Further analyses confirmed that theCa.Allocryptoplasma of ticks, theCa.Allocryptoplasma of lizards and someAnaplasma-like bacteria of wild mice cluster into a monophyletic genus, divergent from all other genera of the family Anaplasmataceae.CandidatusAllocryptoplasma appears as a sister genus ofAnaplasmaand, with the generaEhrlichiaandNeoehrlichia, they form a monophyletic subgroup of Anaplasmataceae associated with tick-borne diseases. The detection of genetically distinctCa.Allocryptoplasma in ticks of significant medical or veterinary interest supports the hypothesis that it is an emergent genus of tick-borne pathogens of general concern.