Desert locusts (Schistocerca gregaria) show a dramatic form of socially induced phenotypic plasticity known as phase polyphenism. In the absence of conspecifics, locusts occur in a shy and cryptic solitarious phase. Crowding with conspecifics drives a behavioural transformation towards gregariousness that occurs within hours and is followed by changes in physiology, colouration and morphology, resulting in the full gregarious phase syndrome. We analysed methylation-sensitive amplified fragment length polymorphisms (MS-AFLP) to compare the effect of acute and chronic crowding on DNA methylation in the central nervous system. We find that rearing the offspring of gregarious-phase locusts in social isolation causes pronounced differentiation of the neuromethylome within an individual's life-time. Crowding isolation-reared locusts for a day, however, has no significant effect on their MS-AFLP fingerprint. The differentiation of the neuromethylome seen in long-term gregarious locusts is therefore unrelated to the acquisition and expression of gregarious behaviour, suggesting that it serves to consolidate long-term phase state.