Abstract Parasitoid wasps are a large group of species‐rich superfamilies within the order Hymenoptera which form an essential part of terrestrial ecosystems. Many species hold additional value as natural enemies of agricultural pests. Considering their ecological and economic importance, it is perhaps surprising that a significant proportion of these insects are understudied. Here we focus on one genus of parasitoid wasp, Syntretus , due to its parasitism of short‐haired bumblebee ( Bombus subterraneus ) queens from Sweden, investigated as part of a reintroduction programme in the United Kingdom (UK). We used a genome‐skimming approach to recover mitochondrial and nuclear DNA from single legs of Syntretus museum specimens, to elucidate the metagenomic content of archival samples and assess their suitability for use in phylogenetic analysis. Utilising 6.7 kb of genomic DNA, we recovered two clades within Syntretus , a possible consequence of host choice. Our analyses also recovered commensal polydnavirus sequences, which is the first time this endogenous virus has been identified in this parasitoid genus. These commensal virions are likely used by egg‐laying female Syntretus to circumnavigate host immune responses so that larvae can develop. Our polydnavirus Bayesian phylogeny suggests that the viral genomes may have different evolutionary histories to their Syntretus hosts, which we infer from the lack of support for co‐speciation in this symbiosis. Finally, we elucidate a novel host‐parasitoid relationship by identifying that S. politus parasitises B. subterraneus in Sweden. Combined, our results demonstrate the value of museum collections in undertaking detailed host‐parasitoid studies, which can, in turn, inform conservation strategies.

DNA from museum samples of a parasitoid wasp genus (Braconidae: Syntretus) offers novel insights into host‐parasitoid interactions