Climate change will alter precipitation patterns with consequences for soil C cycling. An understanding of how fluctuating soil moisture affects microbial processes is therefore critical to predict responses to future global change. We investigated how long-term experimental field drought influences microbial tolerance to lower moisture levels (“resistance”) and ability to recover when rewetted after drought (“resilience”), using soils from a heathland which had been subjected to experimental precipitation reduction during the summer for 18 years. We tested whether drought could induce increased resistance, resilience, and changes in the balance between respiration and bacterial growth during perturbation events, by following a two-tiered approach. We first evaluated the effects of the long-term summer drought on microbial community functioning to drought and drying–rewetting (D/RW), and second tested the ability to alter resistance and resilience through additional perturbation cycles. A history of summer drought in the field selected for increased resilience but not resistance, suggesting that rewetting after drought, rather than low moisture levels during drought, was the selective pressure shaping the microbial community functions. Laboratory D/RW cycles also selected for communities with a higher resilience rather than increased resistance. The ratio of respiration to bacterial growth during D/RW perturbation was lower for the field drought-exposed communities and decreased for both field treatments during the D/RW cycles. This suggests that cycles of D/RW also structure microbial communities to respond quickly and efficiently to rewetting after drought. Our findings imply that microbial communities can adapt to changing climatic conditions and that this might slow the rate of soil C loss predicted to be induced by future cyclic drought.