Distinct strategies associated with colour morphs can have effects on population dynamics, and on the partitioning and population structure of genetic variation. Antagonistic interactions and hybrid incompatibilities between morphs could have negative consequences for population fitness, and its effects may be magnified in a small population. Therefore, covariation between colour and sexual, behavioural and physiological traits may be relevant to conservation management. The Gouldian finch (Erythrura gouldiae) has two sympatric head colour morphs, and with a history of population declines this species is a flagship for conservation in Northern Australia. Captive studies have shown that the sympatric colour morphs correspond to different behavioural strategies, and interbreeding between morphs leads significant offspring mortality. This selection on head colour polymorphism may be a detriment to recovery of Gouldian finch populations, and could lead to genetic substructuring with respect to colour morph. We explore population structure and selection on head colour using traditional population genetics and a recently developed novel marker that determines the underlying genotype for head-colour. We demonstrate the utility of this marker to examine hypotheses with respect to selection on head colour and incompatibility. Across five geographically disparate sampling localities there is evidence of extensive gene-flow between them and between colour morphs. Gene-flow and head-colour frequencies suggest that incompatibility between colour morphs is not a threatening process in the wild.