In non-permanent parasites, host detachment should take place in an environment that ensures the continuation of their life cycle. Timing of detachment - in combination with the host's space use - affects dispersal and transmission success of the parasites and of the pathogens they vector. Before reaching the adult reproductive stage, ticks need to go through multiple immature developmental stages (larva and nymph), each feeding on host blood. In between the feeding bouts, they often remain in the off-host environment for considerable periods of time. With this study, we aimed to obtain more insight in Ixodes frontalis’ off-host habitat use by comparing its detachment pattern in different life stages with that of two habitat-specialized ticks also found on birds: the endophilic tree-hole tick (Ixodes arboricola) and the exophilic sheep tick (Ixodes ricinus), the latter living in humid understory vegetation of forests. For this, we artificially infested hole-roosting (great tits, Parus major) and open-roosting (blackbirds, Turdus merula) birds with ticks under laboratory conditions, and recorded whether detachment occurred during the day or the night. We hypothesize that nocturnal detachment improves off-host mating opportunities and host localization, whereas diurnal detachment optimizes tick dispersal. Ixodes frontalis nymphs detached during the night, especially when feeding on blackbirds. This behaviour was very similar to that of I. arboricola (larva and nymph) feeding on great tits. In contrast, I. frontalis larvae detached during the day, especially when feeding on great tits, which resembles that of I. ricinus’ feeding behaviour (larva and nymph). Ixodes frontalis left the host within seven days, immediately after completion of the blood meal. This is similar to both developmental stages of I. ricinus but contrasts with the very long (up to 20 days) feeding duration in I. arboricola. Thus I. frontalis shows strong plasticity, switching from dispersal-centered (larvae) to host-centered (nymphs) detachment behaviour. Findings are discussed with regard to the ticks’ habitat use, dispersal, life history and host specificity.