The wide geographic and climatic range of the tick Ixodes ricinus, and the consequent marked variation in its seasonal population dynamics, have a direct impact on the transmission dynamics of the many pathogens vectored by this tick species. We use long-term observations on the seasonal abundance and fat contents (a marker of physiological ageing) of ticks, and contemporaneous microclimate at three field sites in the UK, to establish a simple quantitative framework for the phenology (i.e. seasonal cycle of development) of I. ricinus as a foundation for a generic population model. An hour-degree tick inter-stadial development model, driven by soil temperature and including diapause, predicts the recruitment (i.e. emergence from the previous stage) of a single cohort of each stage of ticks each year in the autumn. The timing of predicted emergence coincides exactly with the new appearance of high-fat nymphs and adults in the autumn. Thereafter, fat contents declined steadily until unfed ticks with very low energy reserves disappeared from the questing population within about 1 year from their recruitment. Very few newly emerged ticks were counted on the vegetation in the autumn, but they appeared in increasing numbers through the following spring. Larger ticks became active and subsequently left the questing population before smaller ones. Questing tick population dynamics are determined by seasonal patterns of tick behaviour, host-contact rates and mortality rates, superimposed on a basal phenology that is much less complex than has hitherto been portrayed.