The restriction of effective insecticides has facilitated the woolly apple aphid (WAA) Eriosoma lanigerum to become a major pest in apple orchards in Western Europe. It has also promoted alternative control strategies such as the use of entomopathogenic nematodes (EPN). We evaluated the control capacity of six commercially available EPN, viz. Heterorhabditis bacteriophora, Heterorhabditis megidis, Steinernema carpocapsae, Steinernema feltiae, Steinernema glaseri and Steinernema kraussei. We assessed the potential of these EPN to colonize and parasitize E. lanigerum in an in vitro multiwell test. Only S. carpocapsae caused higher mortality (20–40%) than the control treatment (water). However, the mortality observed with S. carpocapsae was found to be a test artefact and not induced by its specific entomopathogenic activity. A similar mortality range was recorded when applying the non-entomopathogenic nematode Pratylenchus thornei in the same multiwell test set-up. This result warrants careful interpretation of parasitism in these artificial test conditions. The failure of EPN activity was supported in further experiments by frequently finding S. carpocapsae inside living WAA. The presence of the EPN had no effect on aphid reproduction as numbers of ‘large’ embryos in EPN-colonized and non-colonized females were similar. In addition, the dauer juveniles did not recover in E. lanigerum reflecting that S. carpocapsae could not develop inside the WAA. We further demonstrated that growth of the EPN-symbiotic bacteria Xenorhabdus nematophila and Photorhabdus luminescens is inhibited by the body fluid of the WAA, and we speculate that this antibacterial activity is the cause of the unsuccessful parasitization of the WAA by the EPN. This antibiosis inside the body of E. lanigerum would prevent production of the endotoxins by the bacterial symbionts that are essential for entomopathogenicity and insect control.