Socially monogamous birds pursuing extra-pair reproductive strategies may be in conflict, both sexes seeking new mates or copulations outside the pair, while simultaneously attempting to prevent infidelity by the partner. Intra-pair conflicts are augmented by inter-pair conflicts when pairs meet, when all four individuals may be sexually attracted to one member of the other pair while seeking to prevent their mate from copulating, or deserting, with the other. We studied the dynamics, signalling and resolution of these conflicts in a field experiment with the harlequin duck, recording responses to single model birds of both sexes, and to model pairs. Both sexes mate guarded by placing themselves between the mate and a model competitor, and by signalling with the head nod display. Females were closer to model pairs than their mates. Female mate guarding responded adaptively to infidelity risk, increasing to models of paired females, single females and single females inviting copulation, respectively. Males head nodded to signal the goal of (extra-pair) copulation, pairing or mate switching. Courtship by unpaired males increased to models of paired females, single females and single females inviting copulation, respectively. Paired males courted these models equally, perhaps inhibited by the parallel increase in mate guarding of their mates. Males signalled mate guarding using the head nod more than females, but this predicted difference in mate guarding was not shown for the measure of relative proximity to the models. In spite of male extra-pair courtship the harlequin is strictly monogamous, due to female fidelity and close mate guarding. The use of models revealed mate guarding by females, and failed extra-pair reproductive attempts by males, neither of which were apparent from observational studies alone.