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•The subgenus Alloceraeamay be the sister to the other subgenera of the genus Haemaphysalis.•Haemaphysalis(Al.) inermisand H. (Al.) kitaokaiwere well removed from the rest of the Haemaphysalisspecies in our phylogenies.•Haemaphysalis(Al.) inermishad an insertion of 132-bp in the mt genome between the tRNA-Glu (E) gene and the nad1protein-coding gene.•Either Africaniella transversaleor Robertsicus elaphensis, or perhaps Africaniella transversaleplus Ro. elaphensis, are the sister-group to the rest of the metastriate Ixodida.•The “structurally primitive”, “structurally intermediate” and “structurally advanced” Haemaphysalisgroups of Hoogstraal and Kim (1985) do not appear to be monophyletic.•Our amino-acid dataset had Archaeocroton sphenodontias the sister to Ha. (Al.) inermisand Ha. (Alloceraea) kitaokai.•Alectorobius capensisfrom Japan had a higher pairwise (%) genetic-identity to A. sawaiithan to the other A. capensisticks from South Africa; the A. capensisspecimens we sequenced from Japan may be from a cryptic species with respect to the Alectorobius capensisfrom South Africa.