A Bursaphelenchus species was isolated from an ambrosia beetle, Xyleborus seriatus, during a biodiversity survey of entomophilic nematodes in a conserved forest in the Shirakami mountain range, Aomori, Japan. The nematode has several interesting morphological characters that do not fit the morphological definition of Bursaphelenchus, e.g., males have a tail spike instead of a bursal flap and lack the P1 ventral single papilla, and females have a very long and tapering tail (filiform). The molecular phylogenetic status of the new species inferred by the near-full-length small subunit (SSU: 18S) and the D2/D3 expansion segments of the large subunit (LSU: 28S) suggests, however, that the nematode is included in the B. fungivorus group, and is most closely related to B. thailandae and B. willibaldi. Despite these unique morphological characters, its spicule morphology, which is almost identical to that of B. gonzalezi, B. thailandae and B. willibaldi, and vulval structure, i.e., lacking a vulval flap, are in accordance with the molecular phylogenetic status of the nematode. The new species, which shows evidence of secondary loss of the bursal flap and P1 papilla, is described herein as B. kiyoharai n. sp. The typological descriptions of the genus and Parasitaphelenchinae were reconsidered and the taxonomic framework of the Aphelenchoidinae and Parasitaphelenchinae revised. Bursaphelenchus asiaticus n. comb. is proposed for Ruehmaphelenchus asiaticus.