In many species, both parents partake in aggressively defending their territory and offspring from intruders. The costs and benefits of this parental investment can vary between the sexes and are likely to shift over the breeding cycle. However, temporal and sex-specific changes in territory defence are currently poorly understood. To redress this gap, we experimentally investigated territory defence in a colour polymorphic biparental fish, the red devil cichlid (Amphilophus labiatus). We presented either gold or dark coloured conspecific models (i.e. dummies) to A. labiatus pairs at three key stages during the breeding cycle (i.e. after pair formation, after eggs have been laid, and when fry were free-swimming). We found that the sexes differed in their pattern of investment in territorial defence. Males were more aggressive when the pair first formed, whereas females significantly increased their territory defence with time, and were most aggressive when fry were free swimming. Hence, the results show that parental roles in territorial defence can markedly shift over key stages of the breeding cycle. We also found that although the colour of the intruder did not influence the level of aggression by the parents, the colour of the parents themselves did have an effect, with the investment in territory defence being more male biased when the male was of the dark morph. Together our results suggest that the sexes in a pair invest in territorial defence when it most profitable for them, but also importantly that the relative share of aggression in regard to territorial defence is colour-dependant.