Phenotypic plasticity has important ecological and evolutionary consequences. In particular, behavioural phenotypic plasticity such as adaptive foraging (AF) by consumers, may enhance community stability. Yet little is known about the ecological conditions that favor the evolution of AF, and how the evolutionary dynamics of AF may modulate its effects on community stability. In order to address these questions, we constructed an eco-evolutionary model in which resource and consumer niche traits underwent evolutionary diversification. Consumers could either forage randomly, only as a function of resources abundance, or adaptatively, as a function of resource abundance, suitability and consumption by competitors. AF evolved when the niche breadth of consumers with respect to resource use was large enough and when the ecological conditions allowed substantial functional diversification. In turn, AF promoted further diversification of the niche traits in both guilds. This suggests that phenotypic plasticity can influence the evolutionary dynamics at the community-level. Faced with a sudden environmental change, AF promoted community stability directly and also indirectly through its effects on functional diversity. However, other disturbances such as persistent environmental change and increases in mortality, caused the evolutionary regression of the AF behaviour, due to its costs. The causal relationships between AF, community stability and diversity are therefore intricate, and their outcome depends on the nature of the environmental disturbance, in contrast to simpler models claiming a direct positive relationship between AF and stability.