The development of insecticide-resistance mechanisms in aphids has been associated with inhibitory, pleiotropic fitness costs. Such fitness costs have not yet been examined in the UK’s most damaging cereal aphid, Sitobion avenae (grain aphid) (Hemiptera: Aphididae). This study aimed to evaluate the fitness trade-offs of the insecticide-resistant S. avenae clone versus an insecticide-susceptible S. avenae clone. Additionally, the parasitoid, Aphidius ervi (Hymenoptera: Braconidae), was introduced to examine its potential as a biological control agent. This study found that insecticide-resistant clones had significantly lower population growth and individual relative growth rate. Furthermore, insecticide-resistant clones suffered from a significantly greater rate of parasitisation (mummification) compared to their insecticide-susceptible counterparts. The successfulness of the parasitoid as a biological control agent could prevent the spread of the insecticide-resistant genotype. However, for this to be possible, insecticide spraying regimes need to be moderated, and habitat modification and parasitoid manipulation must be considered.