Drought imposes stress on plants and associated soil microbes, inducing coordinated adaptive responses, which can involve plant–soil signalling via phytohormones. However, we know little about how microbial communities respond to phytohormones, or how these responses are shaped by chronic (long-term) drought. Here, we added three phytohormones (abscisic acid, 1-aminocyclopropane-1-carboxylic acid, and jasmonic acid) to soils from long-term (25-year), field-based climate treatments to test the hypothesis that chronic drought alters soil microbial community responses to plant stress signalling. Phytohormone addition increased soil respiration, but this effect was stronger in irrigated than in droughted soils and increased soil respiration at low phytohormone concentrations could not be explained by their use as substrate. Thus, we show that drought adaptation within soil microbial communities modifies their responses to phytohormone inputs. Furthermore, distinct phytohormone-induced shifts in microbial functional groups in droughted vs. irrigated soils might suggest that drought-adapted soil microorganisms perceive phytohormones as stress-signals, allowing them to anticipate impending drought.