Earth’s biosphere has undergone major changes through the last 66 million years, first as terrestrial and marine ecosystems recovered from the devastating Cretaceous/Paleogene (K/Pg; 66 Ma) mass extinction and second as life responded to the profound greenhouse to icehouse climate shift across the Eocene/Oligocene transition (EOT; ~34 Ma). This step change in global climate, saw a switch from warm, high CO₂ greenhouse conditions of the early Paleogene to cooler temperatures, ice sheets and frigid polar water masses of the Oligocene coolhouse. Despite these profound changes we have limited understanding of the relationships between climate and biosphere and in detail how key ecosystem services and functions respond over different timescales of environmental change. Here we use the fossil remains of primary producer ocean plankton (calcareous nannoplankton) to reconstruct community dynamics across this pivotal interval of Earth history. We present a new high-resolution long-time-series middle Eocene to Lower Miocene (45–21 Ma) nannoplankton dataset, combined with complementary published Paleocene to lower Eocene data, to provide a high-fidelity record of biotic response from the base of the marine food web. This 44-million-year record demonstrates a remarkably enduring ‘background’ state of nannoplankton community stability that emerged around two million years after the K/Pg mass extinction event. This stable state was then only periodically interrupted by short lived excursions of high variance that occurred during geologically rapid warming and cooling events. These ephemeral community perturbations show threshold and scaling relationships, triggered by environmental events broadly equivalent to >~2–3 °C of warming or cooling, with volatility of temperature sensitive taxa underpinning the above-background responses regardless of the background climate state (i.e., greenhouse or icehouse). Community stability, resilience and function are likely sustained through high levels of taxonomic redundancy and the long-term dominance of several key species-complexes that have high adaptive genetic potential across vast global populations, which are maintained in their superabundant extant counterparts.