The primary function of animal nests is to protect developing offspring from hostile and fluctuating environments. Animal builders have been shown to adjust nest construction in response to changes in their environment. However, the extent of this plasticity, and its dependence on an evolutionary history of environmental variability, is not well understood. To test whether an evolutionary history with flowing water impacts the male ability to adjust nests in response to a flow regime, we collected three-spined sticklebacks (Gasterosteus aculeatus) from three lakes and three rivers and brought them into reproductive condition in controlled laboratory aquaria. Males were then allowed to nest under both flowing and static conditions. Nest building behaviour, nest structure, and nest composition were all recorded. In comparison to males building nests under static conditions, males building in flowing water took longer to construct their nests and invested more in nesting behaviour. Moreover, nests built in flowing water contained less material and were smaller, more compact, neater, and more elongated than nests built under static conditions. Whether males came from rivers or lakes had little impact on nesting activities, or male capacity to adjust behaviours in response to flow treatment. Our findings suggest that aquatic animals which have experienced a stable environment over a long period of time retain plasticity in nest-building behaviours that allow them to adjust nests to ambient flow conditions. This ability may prove crucial in coping with the increasingly unpredictable flow regimes found in anthropogenically altered waterways and those resulting from global climate change.