Over the past three decades over two hundred species of bird have been the focus of the molecular study of genetic polyandry. I will review this collection of work identifying a number of key characteristics of genetic polyandry in birds, as well as pointing out some serous gaps and biases in the data collected to date. Whilst many recent papers have highlighted ‘controversies’ and a ‘lack of consensus’ in understanding the function of extra-pair paternity, in fact there are a number of relatively well-supported findings. For example, within a population level, nearest neighbours are commonly found to gain extra-pair offspring, and extra-pair paternity is often associated with male age, and the genetic similarity of breeding adults to each other. I believe the latter result highlights the area deserving most future attention – how the genetic structure of populations is likely to affect polyandry. I will argue that selection for compatible genotypes is strong across a number of contexts at the landscape level, and is likely to be an important, and easily over-looked, driver of variation in polyandry. Future studies of genetic polyandry in animals need to consider the nature of selection on genetic compatibility in the broader ecological context which includes the genetic viscosity of populations and the presence of sub-species or sister species. I will present some of our recent laboratory work on a number of species of estridid finch, and focused on sperm trapped in the peri-vitelline membrane, that highlights some of the techniques that may be useful in addressing the challenge of understanding how the broader genetic landscape affects individual behaviour.