Ecosystems can undergo sudden shifts to undesirable states, but recent studies with simple single-species ecosystems have demonstrated that advance warning can be provided by the slowing down of population dynamics near a tipping point. However, it is unclear how this ‘critical slowing down’ will manifest in ecosystems with strong interactions between their components. Here we probe the dynamics of an experimental producer-freeloader ecosystem as it approaches a catastrophic collapse. Surprisingly, the producer population grows in size as the environment deteriorates, highlighting that population size can be a misleading measure of ecosystem stability. By analysing the oscillatory producer-freeloader dynamics for over 100 generations in multiple environmental conditions, we find that the collective ecosystem dynamics slow down as the tipping point is approached. Analysis of the coupled dynamics of interacting populations may therefore be necessary to provide advance warning of collapse in complex communities.Templeton Foundation. Foundational Questions in Evolutionary Biology (Grant RFP-12-07)National Institutes of Health (U.S.) (Grant NIH DP2)National Institutes of Health (U.S.) (Grant R00 GM085279-02)National Science Foundation (U.S.) (Grant PHY-1055154)Pew Charitable TrustsAlfred P. Sloan FoundationPaul Allen Foundation