Growing evidence that individuals of many generalist animals behave as resource specialists has attracted research interest for its ecological and evolutionary implications. Although variation in resource preferences is critical for developing a general theory of individual specialization, it remains to be shown whether diverging preferences can arise among individuals sharing a similar environment and whether these are stable enough to be ecologically relevant. We addressed these issues by means of common garden experiments in feral pigeons (Columba livia), a species known to exhibit resource specialization in the wild. Food-choice experiments on wild-caught pigeons and their captive-bred descendants showed that variation in food preferences can easily arise within a population and that this variation may represent a substantial fraction of the population niche. However, a cross-fostering experiment revealed that the genetic and early common-environment components of food preferences were low, reducing their stability and eroding niche variation in the long-term.