Malaria parasites can affect vector-related behaviours, increasing transmission success. Using Anopheles gambiae and Plasmodium falciparum, we consider the effect of interaction between infection stage and vector age on diel locomotion in response to human odour and the expression of antennal chemosensory genes. We demonstrate age-dependent behavioural diel compartmentalisation by uninfected females. Infection disrupts overall and diel activity patterns compared with age-matched controls. Mosquitoes carrying transmissible sporozoites are more active, shifting activity periods to coincide with human host availability, in response to human odour. Older, uninfected females reduce activity during their peak host-seeking period in response to human odour. Age- and infection stage-specific changes in odour-mediated locomotion coincide with altered transcript abundance of select chemosensory genes providing a possible molecular mechanism regulating the behaviour. Our results support the hypothesis that vector-related behaviours of female mosquitoes are altered by infection stage and further modulated by the age of the vector, and have important implications for malaria transmission and disease dynamics.