We used a common-garden rearing experiment to explore environmentally induced tolerance to hypoxia in the African mouth-brooding cichlid Pseudocrenilabrus multicolor. F(1) fish originating from three field populations were grown under low or high dissolved oxygen (DO), and their resting routine metabolic rate (RMR), critical oxygen tension (P(crit)), and marginal metabolic scope (MMS) were quantified. In a second rearing experiment, we compared the RMR of brooding and nonbrooding females of low-DO origin grown under low and high DO. Fish reared under low DO had a lower P(crit) than fish reared under high DO. There was also an interaction between treatment and gender; females had a higher P(crit) than males when reared under normoxia. Variation in RMR was driven primarily by population effects, and there was an interaction between treatment and population. Regardless of population or treatment, males had a higher MMS than females. Fish reared under low DO had a higher MMS than fish reared under high DO, except for the high-DO population in which there was no treatment effect. Brooding females had a higher RMR than postbrooding females regardless of the growth treatment, indicating an energetic cost to brooding. The results suggest a strong element of developmental plasticity in P(crit) across populations and both plastic and genetic components of variation in the RMR and MMS. This study also highlights the cost of parental care in mouth-brooding fishes, which may increase the fitness of the offspring at the energetic expense of the parent, a cost that may be elevated under hypoxia.