The increase of extreme drought and precipitation events due to climate change will alter microbial processes. Perturbation experiments demonstrated that microbes are sensitive to environmental alterations. However, only little is known on the legacy effects in microbial systems. Here, we designed a laboratory microcosm experiment using aerobic methane-consuming communities as a model system to test basic principles of microbial resilience and the role of changes in biomass and the presence of non-methanotrophic microbes in this process. We focused on enrichments from soil, sediment, and water reflecting communities with different legacy with respect to exposure to drought. Recovery rates, a recently proposed early warning indicator of a critical transition, were utilized as a measure to detect resilience loss of methane consumption during a series of dry/wet cycle perturbations. We observed a slowed recovery of enrichments originating from water samples, which suggests that the community’s legacy with a perturbation is a contributing factor for the resilience of microbial functioning. © 2018 The Author(s).