Northern peatlands have accumulated one third of the Earth's soil carbon stock since the last Ice Age. Rapid warming across northern biomes threatens to accelerate rates of peatland ecosystem respiration. Despite compensatory increases in net primary production, greater ecosystem respiration could signal the release of ancient, century- to millennia-old carbon from the peatland organic matter stock. Warming has already been shown to promote ancient peatland carbon release, but, despite the key role of vegetation in carbon dynamics, little is known about how plants influence the source of peatland ecosystem respiration. Here, we address this issue using in situ 14C measurements of ecosystem respiration on an established peatland warming and vegetation manipulation experiment. Results show that warming of approximately 1 °C promotes respiration of ancient peatland carbon (up to 2100 years old) when dwarf-shrubs or graminoids are present, an effect not observed when only bryophytes are present. We demonstrate that warming likely promotes ancient peatland carbon release via its control over organic inputs from vascular plants. Our findings suggest that dwarf-shrubs and graminoids prime microbial decomposition of previously ‘locked-up’ organic matter from potentially deep in the peat profile, facilitating liberation of ancient carbon as CO2. Furthermore, such plant-induced peat respiration could contribute up to 40% of ecosystem CO2 emissions. If consistent across other sub-arctic and arctic ecosystems, this represents a considerable fraction of ecosystem respiration that is currently not acknowledged by global carbon cycle models. Ultimately, greater contribution of ancient carbon to ecosystem respiration may signal the loss of a previously stable peatland carbon pool, creating potential feedbacks to future climate change.