1. The epidemiology of sexually transmitted diseases (STDs) in human and domesticated populations is well documented. However, there has been less study of STDs in natural populations. 2. We investigated STD dynamics in the model system involving a host from the most speciose group of animals: the insects. We investigated temporal variation in the prevalence of the sexually transmitted mite Coccipolipus hippodamiae on its ladybird host, Adalia bipunctata. 3. Field surveys over two seasons showed a repeated pattern of a profound epidemic in the overwintered cohort and a later prevalence decline. 4. In order to understand the key factors in the dynamics of this system we studied the phenology of the host and simulated parasite dynamics in the overwintered cohort using a model with within-sex homogeneity in mating rate and field-measured parameter values. The similarity of natural and simulation prevalence levels allowed us to carry out sensitivity analysis and hence to identify the key determinants of the dynamics. 5. The observed pattern of periodic extreme prevalence combined with system persistence probably results from time lags in host recruitment and widespread promiscuity. 6. Our findings improve our understanding of STDs in natural populations and illustrate the importance of examining seasonality and time delays in population dynamics in order to fully understand the characteristics of natural populations and their parasites.