AbstractAimHost specificity within plant‐feeding insects constitutes a fascinating example of natural selection that promotes inter‐specific niche segregation. If specificity is strong, composition of local plant parasitic insect guilds is largely dependent on the presence and prevalence of the preferred hosts. Alternatively, if it is weak or absent, historic and stochastic demographic processes may drive the structuring of insect communities. We assessed whether the species composition of acorn feeding insects (Curculio spp. guilds) and their genetic variation change geographically according to the local host community.LocationAn 800 km transect across California, USA.MethodsWe used DNA taxonomy to detect potential Curculio cryptic speciation and assessed intra‐specific genetic structure among sampling sites. We monitored larval performance on different hosts, by measuring the weight of each larva upon emerging from the acorn. Our phylogenetic and spatial analyses disentangled host specificity and geographical effects on Curculio community composition and genetic structure.ResultsDNA taxonomy revealed no specialized cryptic species. Californian Curculio spp. were sister taxa that did not segregate among Quercus species or, at a deeper taxonomic level, between red and white oaks. Curculio species turnover and intra‐specific genetic differentiation increased with geographical distance among localities irrespective of local oak species composition. Moreover, larval performance did not differ among oak species or acorn sizes when controlling for the effect of the locality.Main conclusionsHistorical processes have contributed to the structuring of acorn weevil communities across California. Trophic niche overlapped among species, indicating that ecologically similar species can co‐exist. Acorn crop inter‐annual variability and unpredictability in mixed oak forests may have selected against narrow specialization, and facilitated co‐existence by means of an inter‐specific time partitioning of the resources. Wide‐scale geographical records of parasitic insects and their host plants are necessary to understand the processes underlying species diversity.