In temperate regions, many vector-borne parasites maximise their transmission prospects by adjusting reproduction to seasonal cycles of host susceptibility and vector availability. Nevertheless, in these regions there are areas where environmental conditions are favourable throughout the year, so that parasites could benefit from a year-round transmission strategy. We analysed how different transmission strategies (strict summer transmission, extended summer transmission - including spring and autumn, and year round transmission) have evolved among the different genetic lineages of Haemoproteus parabelopolskyi, an avian blood-borne parasite shared by three sibling species of passerine hosts. Our results indicate that the ancestral state of this clade of parasites had a strict summer transmission with the blackcap (Sylvia atricapilla) as the host. Other transmission strategies and switches to the other host species (Sylvia abyssinica and Sylvia born) evolved recently, several times, independently. This suggests that, although year-round transmission is ecologically successful at present, seasonal transmission may have become more stable over evolutionary time. Switches from strict summer to an extended or year-round transmission strategy could have ecological consequences, if they promote the spread of parasites into more distant regions, transported by the migrating bird hosts. Therefore, a deeper knowledge of how different parasite transmission strategies are structured among birds in temperate areas is essential for understanding how disease emergence risks may develop in the future. (C) 2015 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.