Circadian rhythms optimize health by coordinating the timing of physiological processes to match predictable daily environmental challenges. The circadian rhythm of body temperature is thought to be an important modulator of molecular clocks in peripheral tissues, but how daily temperature cycles affect physiological function is unclear. Here, we examined the effect of constant temperature (Tcon, 25°C) and cycling temperature (Tcyc, 28°C:22°C during light:dark) paradigms on lifespan of Drosophila melanogaster, and the expression of clock genes, heat shock protein 83 (Hsp83), Frost (Fst) and senescence marker protein-30 (smp-30). Male and female D. melanogaster housed at Tcyc had longer median lifespans than those housed at Tcon. Tcyc induced robust Hsp83 rhythms and rescued the age-related decrease in smp-30 expression that was observed in flies at Tcon, potentially indicating an increased capacity to cope with age-related cellular stress. Ageing under Tcon led to a decrease in the amplitude of expression of all clock genes in the bodies of male flies, except for cyc, which was non-rhythmic, and for per and cry in female flies. Strikingly, housing under Tcyc conditions rescued the age-related decrease in amplitude of all clock genes, and generated rhythmicity in cyc expression, in the male flies, but not the female flies. The results suggest that ambient temperature rhythms modulate D. melanogaster lifespan, and that the amplitude of clock gene expression in peripheral body clocks may be a potential link between temperature rhythms and longevity in male D. melanogaster. Longevity due to Tcyc appeared predominantly independent of clock gene amplitude in female D. melanogaster.