Abstract One way to cope with predictable environmental fluctuations that affect several generations of individuals is through nongenetic transgenerational effects. Ancestors match the phenotype of their descendants to the environment the latter are expected to experience. In facultatively sexual rotifer life cycles, sex is linked to the production of diapausing eggs, which enables survival between growing seasons. In some rotifer species, sexual reproduction is inhibited several generations after diapausing eggs hatch. We hypothesised that in ponds where the growing season length is predictable, rotifer clones reproduce asexually for more generations, allowing a fuller exploitation of the growing season and maximising production of diapausing eggs at the end of the season. We tested this prediction by estimating the proportion of sexual females produced by several clones of the rotifer Brachionus plicatilis inhabiting eight ponds that vary in the predictability of the length of their growing season. Rotifer clones from more predictable ponds were unresponsive to cues that induce sexual reproduction for more generations after leaving diapause than clones from unpredictable ponds. However, clones from more unpredictable ponds did respond to these cues from early generations, probably as a way to ensure the production of diapausing eggs against the risk of an unexpectedly early end to the growing season. Significant within‐population clonal variation was observed in transgenerational responses. Our results showed that the transgenerational inhibition of sexual reproduction observed in B. plicatilis evolved in clones from habitats where the length of the growing season (i.e., the period when populations are active in the water column) is more predictable on an interannual scale. Our findings also suggest that the longer the growing season, the more prolonged the inhibition effect (i.e., it affects a greater number of asexual generations). This research shows the importance of understanding how organisms adapt to fluctuating environments through transgenerational strategies and establishes the groundwork for future studies of the regulatory mechanisms underlying the transgenerational modulation of sex in rotifers.