Ixodes apronophorusis an insufficiently studied nidicolous tick species. For the first time, the prevalence and genetic diversity ofRickettsiaspp. inIxodes apronophorus,Ixodes persulcatus, andIxodes triangulicepsticks from their sympatric habitats in Western Siberia were investigated.Rickettsia helveticawas first identified inI. apronophoruswith a prevalence exceeding 60%. “CandidatusRickettsia tarasevichiae” dominated inI. persulcatus, whereasI. triangulicepswere infected with “CandidatusRickettsia uralica”,R. helvetica, and “Ca. R. tarasevichiae”. For larvae collected from small mammals, a strong association was observed between tick species and rickettsiae species/sequence variants, indicating that co-feeding transmission in studied habitats is absent or its impact is insignificant. Phylogenetic analysis of all availableR. helveticasequences demonstrated the presence of four distinct genetic lineages. Most sequences fromI. apronophorusbelong to the unique lineage III, and single sequences cluster into the lineage I alongside sequences from EuropeanI. ricinusand SiberianI. persulcatus.Rickettsia helveticasequences fromI. trianguliceps, along with sequences fromI. persulcatusfrom northwestern Russia, form lineage II. Other knownR. helveticasequences fromI. persulcatusfrom the Far East group into the lineage IV. The obtained results demonstrated the high genetic variability ofR. helvetica.