Evidence is growing that evolutionary dynamics can impact biodiversity–ecosystem functioning (BEF) relationships. However the nature of such impacts remains poorly understood. Here we use a modelling approach to compare random communities, with no trait evolutionary fine‐tuning, and co‐adapted communities, where traits have co‐evolved, in terms of emerging biodiversity–productivity, biodiversity–stability and biodiversity–invasion relationships. Community adaptation impacted most BEF relationships, sometimes inverting the slope of the relationship compared to random communities. Biodiversity–productivity relationships were generally less positive among co‐adapted communities, with reduced contribution of sampling effects. The effect of community‐adaptation, though modest regarding invasion resistance, was striking regarding invasion tolerance: co‐adapted communities could remain very tolerant to invasions even at high diversity. BEF relationships are thus contingent on the history of ecosystems and their degree of community adaptation. Short‐term experiments and observations following recent changes may not be safely extrapolated into the future, once eco‐evolutionary feedbacks have taken place.