Avian haemosporidians are widespread and diverse and are classified in the genera Plasmodium, Haemoproteus, Leucocytozoon, and Fallisia. These species are known to cause haemosporidiosis and decreased fitness of their hosts. Despite the high diversity of habitats and animal species in Iran, only few studies have addressed avian haemosporidians in this geographic area. This study was performed in the south and southeast of Iran during the bird breeding seasons in 2017 and 2018, with the aim to partly fill in this gap. Blood samples of 237 passerine birds belonging to 41 species and 20 families were collected. Parasite infections were identified using a nested PCR protocol targeting a 479-base-pair fragment of the mitochondrial cytochrome b (cytb) gene of Haemoproteus, Plasmodium and Leucocytozoon species. The overall prevalence of haemosporidian parasites was 51.1%, and 55 different lineages were identified, of which 15 cytb lineages were new globally. The lineages of Haemoproteus predominated (63.6% of all detected lineages), followed by Leucocytozoon and Plasmodium. Nineteen new host records of haemosporidian cytb lineages were identified, and the majority of them were found in resident bird species, indicating local transmission. Thirteen co-infections (9.8% of infected individuals) of Haemoproteus and Leucocytozoon parasites in seven host species were observed. This study shows the presence of active local transmission of parasites to resident bird species in the southeast of Iran and contributes to the knowledge on haemosporidian parasite biodiversity in this poorly studied region of the world.