Pesticide resistance facilitates adaptation and survival through a range of different mechanisms that reduce or diminish the effectiveness of an active ingredient, for example by preventing its mode of action at the target site. Resistance to pyrethroid insecticides detected in 2014 in Sitobion avenae (Fabricius) (Hempitera: Aphididae), a prolific cereal pest and vector of Barley Yellow Dwarf Virus (BYDV), presents a serious challenge to cereal growers. Resistance has been attributed to the classic target site mutation (L1014F) known as Knock Down Resistance (kdr), found on one allele of the aphid sodium channel gene. Resistance screening and microsatellite genotyping over a three year period in Ireland reveals that kdr-heterozygote aphids occur extensively in cereal fields and adjoining grass verges, with resistance predominantly in one SA3 superclone. Furthermore, a second resistance mechanism in the form of pesticide detoxification has been detected in some SA3 clones, likely linked to enhanced cytochrome P450 monooxygenase activity. Resistance mutations are frequently believed to carry fitness penalties. However, our research provides evidence that whilst the heterozygote kdr SA3 S. avenae superclone can survive pyrethroid exposure up to twice the normal field application rate, it continues to be able to reproduce asexually at rates comparable to fully susceptible individuals. Furthermore, under laboratory conditions sexual capacity is retained in the SA3 superclone, with the observation of oviparous morphs, creating the possibility of gene-flow through a wide range of (androcyclic, holocyclic and intermediate) breeding systems, and creation of kdr-homozygote offspring through sexual crossing between kdr-heterozygotes if heterozygote resistant male aphids are produced. These findings have serious implications for resistance management and the future efficacy of pyrethroid insecticides in controlling grain aphids and the associated risk of BYDV transmission in crops.