Migration is a widely observed phenomenon supported by morphological, physiological and behavioural traits that vary with season. Moreover, they also vary between sexes in a wide range of migrant species due to different life-history requirements. Recently studies have unpacked the genetic components underpinning migration in the marmalade hoverfly (Diptera: Syrphidae) by detecting differential gene expression between migrant and non-migrant females. Male hoverflies also migrate, but changing sex ratios during their journeys in autumn, from approximately 50% females in northern Europe to ~90% the south, suggest males are poorer long-distance migrants. To elucidate the mechanisms underpinning this sex difference, we carried out morphological, physiological, and transcriptomic characterisation of actively migrating females and males caught as they traversed a high mountain pass in the Pyrenees. Females and males show similar physiological adaptations to migration such as hyperphagia and resistance to starvation, but females display significantly higher tolerance to cold and hypoxia, up-regulate a suite of immune genes, and have lower wing loading values and a higher flight capacity. In addition, age-related loss of flight muscle size indicates that females are significantly older than male migrants, and transcriptomics indicate that this increased longevity is centred on up-regulation of takeout and the suppression of hormonal pathways maintaining reproductive diapause. These results may be relevant to a swathe of insect migrants that show sex biased migrations and influence population dynamics in many beneficial and pest species world-wide.