Methane (CH₄) is a potent greenhouse gas but also an important carbon and energy substrate for some lake food webs. Understanding how CH₄ incorporates into food webs is, therefore, crucial for unraveling CH₄ cycling and its impacts on climate and ecosystems. However, CH₄-fueled lake food webs from pre-Holocene intervals, particularly during greenhouse climates in Earth history, have received relatively little attention. Here, we present a long-term record of CH₄-fueled pelagic food webs across the Cretaceous Oceanic Anoxic Event 1a (~120 Mya) that serves as a geological analog to future warming. We show an exceptionally strong expansion of both methanogens and CH₄-oxidizing bacteria (up to 87% of hopanoid-producing bacteria) during this Event. Grazing on CH₄-oxidizing bacteria by zooplankton (up to 47% of ciliate diets) within the chemocline transferred substantial CH₄-derived carbon to the higher trophic levels, representing an important CH₄ sink in the water column. Our findings suggest that as Earth warms, microbial CH₄ cycling could restructure food webs and fundamentally alter carbon and energy flows and trophic pathways in lake ecosystems.