The collective behavior and success of social groups is often disproportionately influenced by one or a few key individuals, which we term here “keystone individuals”. Here we explore how the competence of keystone individuals changes the collective learning potential and success of their societies. In the social spider Stegodyphus dumicola, colonies’ boldest individuals wield a disproportionately large influence over colony responsiveness to prey, where colonies containing just one very bold individual attack prey more rapidly and with 400% more attackers. We trained bold (keystone) individuals or shy (generic) individuals to associate two novel vibratory stimuli with either rewarding or unrewarding prey (moths vs. predatory ants). We then placed one knowledgeable individual into a colony with 14 inexperienced, uninformed shy individuals and monitored colony foraging behavior over time in laboratory. Colonies were placed in conditions that either matched (association maintained) or mismatched (reversed association) the training of the one knowledgeable individual in the colony, be it a keystone or generic individual. We found that whether a keystone’s training matched or mismatched its new environment had large consequences on the collective foraging behavior of the society. The training of shy generic individuals always had very little influence. Colonies containing informed keystones, whose training matched their environment, quickly learned to attack the profitable stimulus in large numbers and to avoid the unrewarding stimulus. In contrast, colonies containing misinformed keystones, whose training mismatched their environment, never learned to attack the rewarding stimulus, resulting in massive die-offs within colonies. Thus, the consequences of information quality on societal success depended on the influence of its original bearers, where information quality in the hands of keystones determines whether their colonies flourish or wither.