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Background  For specialised pollinators, the synchrony of plant and pollinator life history is critical to the persistence of pollinator populations. This is even more critical in nursery pollination, where pollinators are obligately dependant on female host plant flowers for oviposition sites.  Epicephala  moths (Gracillariidae) form highly specialised nursery pollination mutualisms with Phyllanthaceae plants. Several hundred Phyllanthaceae are estimated to be exclusively pollinated by highly specific  Epicephala  moths, making these mutualisms an outstanding example of plant–insect coevolution. However, there have been no studies of how  Epicephala  moths synchronise their activity with host plant flowering or persist through periods when flowers are absent. Such knowledge is critical to understanding the ecology and evolutionary stability of these mutualisms. We surveyed multiple populations of both  Breynia oblongifolia  (Phyllanthaceae) and it’s  Epicephala  pollinators for over two years to determine their phenology and modelled the environmental factors that underpin their interactions.    Results  The abundance of flowers and fruits was highly variable and strongly linked to local rainfall and photoperiod. Unlike male flowers and fruits, female flowers were present throughout the entire year, including winter. Fruit abundance was a significant predictor of adult  Epicephala  activity, suggesting that eggs or early instar larvae diapause within dormant female flowers and emerge as fruits mature. Searches of overwintering female flowers confirmed that many contained pollen and diapausing pollinators. We also observed diapause in  Epicephala  prior to pupation, finding that 12% (9/78) of larvae emerging from fruits in the autumn entered an extended diapause for 38–48 weeks. The remaining autumn emerging larvae pupated directly without diapause, suggesting a possible bet-hedging strategy.    Conclusions   Epicephala  appear to use diapause at multiple stages in their lifecycle to survive variable host plant phenology. Furthermore, moth abundance was predicted by the same environmental variables as male flowers, suggesting that moths track flowering through temperature. These adaptations may thereby mitigate against unpredictability in the timing of fruiting and flowering because of variable rainfall. It remains to be seen how widespread egg diapause and pre-pupal diapause may be within  Epicephala  moths, and, furthermore, to what degree these traits may have facilitated the evolution of these highly diverse mutualisms.    Supplementary Information  The online version contains supplementary material available at 10.1186/s12862-021-01889-4.

Staying in touch: how highly specialised moth pollinators track host plant phenology in unpredictable climates