Males may increase their fitness through extra–pair copulations (copulations outside the pair bond) that result in extra–pair fertilizations, but also risk lost paternity when they leave their own mate unguarded. The fitness costs of cuckoldry for Seychelles warblers (Acrocephalus sechellensis) are considerable because warblers have a single–egg clutch and, given the short breeding season, no time for a successful replacement clutch. Neighbouring males are the primary threat to a male's genetic paternity. Males minimize their loss of paternity by guarding their mates to prevent them from having extra–pair copulations during their fertile period. Here, I provide experimental evidence that mate–guarding behaviour is energetically costly and that the expression of this trade–off is adjusted to paternity risk (local male density). Free–living males that were induced to reduce mate guarding spent significantly more time foraging and gained significantly better body condition than control males. The larger the reduction in mate guarding, the more pronounced was the increase in foraging and body condition (accounting for food availability). An experimental increase in paternity risk resulted in an increase in mate–guarding intensity and a decrease in foraging and body condition, and vice versa. This is examined using both cross–sectional and longitudinal data. This study on the Seychelles warbler offers experimental evidence that mate guarding is energetically costly and adjusted to paternity risk.