It has been hypothesized that the 2-year oscillations in abundance of Xestia moths are mediated by interactions with 1-year Ophion parasitoid wasps. We tested this hypothesis by modelling a 35-year time series of Xestia and Ophion from northern Finland. Additionally, we used DNA barcoding to ascertain the species diversity of Ophion and targeted amplicon sequencing of their gut contents to confirm their larval hosts. Modelling of the time-series data strongly supported the hypothesized host–parasitoid dynamics and that periodic occurrence of Xestia moths is mediated by Ophion. DNA barcodes revealed that Ophion included five species rather than just one while targeted amplicon sequencing verified that Ophion does parasitize Xestia. At least one Ophion species employs 1-year Syngrapha interrogationis as an alternate host, but it did not detectably affect Xestia–Ophion dynamics. We also demonstrate the previously unrecognized complexity of this system due to cryptic parasitoid diversity.