Haemoproteus (Haemoproteus) multipigmentatus n. sp. (Haemosporida, Haemoproteidae) was found in the endemic Galapagos dove Zenaida galapagoensis. It is described based on the morphology of its blood stages and segments of the mitochondrial cytochrome b gene, which can be used for molecular identification and diagnosis of this species. Haemoproteus multipigmentatus can be readily distinguished from all species of hemoproteids of the subgenus Haemoproteus, primarily due to numerous (approximately 40 on average) small pigment granules in its mature gametocytes. Illustrations of blood stages of the new species are given, and phylogenetic analysis identifies DNA lineages closely related to this parasite, which is prevalent in the Galapagos dove and also has been recorded in other species of Columbiformes in Mexico, Guatemala, and Peru, and so seems to be widespread in countries in the New World with warm climates. Cytochrome b lineages of H. multipigmentatus cluster with hippoboscid-transmitted lineages of Haemoproteus columbae. The same lineages of H. multipigmentatus were recorded in thoraxes of the hippoboscid fly Microlynchia galapagoensis, which likely is a natural vector of this parasite in Galapagos. Because different primers might amplify different parasites if they have a better match during a simultaneous infection, it is important that researchers standardize the genetic marker of choice for molecular typing of hemosporidian species. This study shows that more discussion among researchers is needed to clearly establish the sequence length and number of genes used for identification of hemosporidian parasites at different taxonomic levels. We point to the need of using both morphology and gene markers in studies of hemosporidian parasites, particularly in wildlife.