Simple SummaryThe meadow spittlebug, Philaenus spumarius is the major vector of Xylella fastidiosa in Europe. The spread of X. fastidiosa depends almost exclusively on insect transmission, and therefore, it is vital to keep vector populations low. To achieve this goal, natural enemies should be identified and their efficacy evaluated. The aim of this work was to assess the presence and abundance of a parasitoid fly, Verrallia aucta, in field-collected spittlebugs. At first, we developed a new species-specific molecular tool (PCR) to identify the parasitoid, then we estimated the parasitization rate in different sites of northern Italy using both PCR and the dissection of insect bodies. Finally, we established a small-scale rearing to describe the life cycle of the fly on its spittlebug host. Verrallia aucta is quite common in northern Italy but displayed low prevalence, reaching a maximum parasitization rate of 17.5% in vineyards of the Piemonte region. The fly has one generation per year, lays eggs in newly emerged adults of spittlebugs, and develops inside the host throughout the summer. The mature larva abandons the dead victim at the beginning of autumn and pupates in the soil where it overwinters.The meadow spittlebug, Philaenus spumarius (L.) (Hemiptera Aphrophoridae), the main vector of Xylella fastidiosa Wells et al. in Europe, has few known natural enemies. The endoparasitoid Verrallia aucta (Fallén) (Diptera, Pipunculidae) was first noticed a long time ago but very little is known about its biology and prevalence. In this study, the presence and prevalence of V. aucta were investigated in different regions of northern Italy, both in plain–foothill and montane zones. Parasitic larvae were identified by the dissection of spittlebug adults, P. spumarius and Neophilaenus campestris (Fallén), and by a new species-specific molecular tool targeting the ITS2 and COI genomic regions, developed in this work. A small-scale rearing was set up to gain information on the life cycle of V. aucta on its main host P. spumarius. During the four-year investigation (2016–2019) the pipunculid parasitoid displayed low prevalence, reaching a maximum parasitization rate of 17.5% (calculated over the adult spittlebug season) in vineyards of the Piemonte region. Over the whole period, no significant difference in the prevalence was found between male and female spittlebugs. Collected data and rearing observations suggest that V. aucta is monovoltine and synchronous with P. spumarius, laying eggs in newly emerged adults, developing as an endoparasitoid through two larval stages during the whole summer, and overwintering as a pupa in the soil.