Desert locusts show a dramatic form of socially induced phenotypic plasticity known as phase polyphenism. In the absence of conspecifics, locusts occur in a lone-living, shy and cryptic solitarious phase. Crowding with other locusts drives a rapid behavioural transformation towards gregarious behaviour that occurs over the span of few hours and is followed by changes in physiology, colouration and morphology to result in the full syndrome of the gregarious phase. We used methylation-sensitive amplified fragment length polymorphism (MS-AFLP) fingerprinting to compare the effect of social isolation, long-term crowding and acute crowding for one day on DNA methylation in the central nervous system. We find that rearing the offspring of chronically crowded locusts in social isolation leads to a 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 pronounced differentiation of the neural methylome 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.