Marine cold seeps sustain one of the most productive chemosynthetic ecosystems on Earth, through which a vast amount of the deeply sourced methane is reintroduced into Earth’s active carbon cycle. While conventional paradigm emphasizes the key role of anaerobic methane oxidation in preventing methane reaching the upper ocean, aerobic methanotrophs often are restricted to the shallow oxygen-penetrating sediments and thought to contribute minorly to methane filtration in cold seeps. By integrating geochemical profiling with Illumina short-read and Oxford Nanopore long-read sequencing, here we reveal the unexpected prevalence of aerobic methanotroph Methyloprofundus throughout the oxic and hypoxic sediment layers of a newly formed methane seep ecosystem in the South China Sea. Three novel species of Methyloprofundus were identified based on robust phylogenomic analyses on the high-quality metagenome-assembled genomes (MAGs). Meta-transcriptomic profiling further indicated persistently high transcriptional activities of Methyloprofundus across the oxic and hypoxic layers using two distinct enzymatic machineries i.e. sMMO and pMMO, respectively. Together these findings demonstrated high metabolic plasticity of Methyloprofundus that enables niche partitioning of distinct species across the oxic -hypoxic gradients, highlighting the overlooked biodiversity of aerobic methanotrophs and their contribution to methane filtration in the highly dynamic early-stage cold seeps.