Early theories of aging suggested that organisms with relatively high metabolic rates would live shorter lives. Despite widespread tests of this ‘rate of living’ theory of aging, there is little empirical evidence to support the idea. A more fine-grained approach that examined age-related changes in metabolic rate over the life span could provide valuable insight into the relationship between metabolic rate and aging. Here we compare age-related metabolic rate (measured as CO2 production per hour) and age-related mortality rate among five species in the genus Drosophila. We find no evidence that longer-lived species have lower metabolic rates. In all five species, there is no clear evidence of an age-related metabolic decline. Metabolic rates are strikingly constant throughout the life course, with the exception of females of D. hydei, in which metabolic rates show an increase over the first third of the life span and then decline. We argue that some physiological traits may have been shaped by such strong selection over evolutionary time that they are relatively resistant to the decline in the force of selection that occurs within the life time of a single individual. We suggest that comparisons of specific traits that do not show signs of aging with those traits that do decline with age could provide insight into the aging process.