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The role of environmental and host-associated factors in synchronization of host–parasite life-cycles is an important question of evolutionary ecology. Yet, only handsome of studies examined this question at the intraspecific level. Here we explore how host-associated traits, such as breeding phenology and host breeding habitat, can influence parasite phenology and co-occurrence at different spatial scales. We studied the system comprised of a generalist ectoparasitic fly Carnus hemapterus and one of its avian hosts, the European roller Coracias garrulus. Inter-annual variation in phenology was larger for parasites than hosts. Host predictability in terms of occurrence and phenological regularity was moderate, suggesting that this resource can be difficult to be tracked by the parasite. A large proportion of flies consistently emerged before the appearance of suitable host resources at both the nest and population level. Consequently, we revealed low and highly variable inter-annual host–parasite synchronization rates. Nevertheless, we found that parasites from nests of early and progressively earlier breeding European rollers were more synchronized with their hosts than parasites from nests of late and progressively later breeding hosts, respectively. Temporal trends in host suitability and parasite emergence at the population scale suggest that other mechanisms, such as dispersal or exploitation of other host species, ensure parasites access to resources and counteract asynchrony with the host at the nest scale.