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Leucocytozoon parasites remain poorly investigated in comparison to other haemosporidians. The host cell inhabited by their blood stages (gametocytes) remains insufficiently known. This study aimed to determine the blood cells inhabited by Leucocytozoon gametocytes in different species of Passeriformes and to test if this feature has a phylogenetic importance. We microscopically analyzed blood films stained with Giemsa from six different bird species and individuals and used PCR-based methods for parasite lineage identification. The DNA sequences obtained were applied for phylogenetic analysis. Leucocytozoon parasite from the song thrush Turdus philomelos (cytochrome b lineage STUR1), the blackbird Turdus merula (undetermined lineage), the garden warbler Sylvia borin (unknown lineage) inhabited erythrocytes, a parasite from the blue tit Cyanistes caeruleus (PARUS4) infects lymphocytes, while in the wood warbler Phylloscopus sibilatrix (WW6) and the common chiffchaff Phylloscopus collybita (AFR205) they were found inhabiting thrombocytes. Parasites infecting thrombocytes were closely related, while the parasites infecting erythrocytes were placed in three different clades, and the one found in lymphocytes was placed in a separate clade. This shows that the determination of host cells inhabited by Leucocytozoon parasites can be phylogenetically important and should be considered in future species descriptions. Noteworthy, phylogenetic analysis might be used for the prediction of which host cells parasite lineages might inhabit.