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Simple Summary: Pathogenic nematode Ostertagia leptospicularis, as the sole member of the subfamily Ostertagiinae, occurs in both cervid and bovid host species. The broad host specificity of this parasite draws special attention and requires a more in-depth investigation. This study was carried out to find out whether the differences in the nematode morphology were only due to the host influence, or whether genetic differences should be taken into account. To resolve this issue, the classification of O. leptospicularis was raised and discussed based on its host specificity, as well as morphological and genetic characteristics. A combined morphological–molecular approach was used to compare specimens resembling O. leptospicularis collected from naturally infected hosts of various ruminant species (roe deer, red deer, fallow deer, and cattle). Both morphological and molecular analyses highlighted the distinctiveness of O. leptospicularis collected from cattle in Germany, and therefore should now be considered to be a different strain that those collected form cervids in central Europe. Ostertagia leptospicularis Assadov, 1953 was formally described in roe deer Capreolus capreolus and has been reported in a wide range of ruminants, including other Cervidae, as well as Bovidae. Nematode specimens derived from various host species exhibit morphological similarity; however, some differences can be observed. It is unclear if this is due to the differential reaction of one nematode species in different host species (i.e., host-induced changes) or because of distinct nematode species in these hosts (i.e., species complex). This paper focuses on specimens resembling O. leptospicularis f. leptospicularis and its closely related species (Ostertagia ostertagi f. ostertagi) collected from various hosts. Morphometric and molecular techniques were applied to assess host-induced changes in nematode morphology and to clarify its systematic classification. There was an overall effect of host species on measurements of nematodes resembling O. leptospicularis (both males and females), but the distinctiveness of the specimens from cattle Bos taurus were highlighted. The results obtained may suggest that the specimens of O. leptospicularis from cattle in Germany and cervids in central Europe belong to different strains. Furthermore, nematodes from the cervid strain appear to circulate within particular host species, which can be seen in the stated morphological variations. [ABSTRACT FROM AUTHOR]