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Antarctic krill (Euphausia superba) is Earth's most abundant wild animal, and its enormous biomass is vital to the Southern Ocean ecosystem. Here, we report a 48.01-Gb chromosome-level Antarctic krill genome, whose large genome size appears to have resulted from inter-genic transposable element expansions. Our assembly reveals the molecular architecture of the Antarctic krill circadian clock and uncovers expanded gene families associated with molting and energy metabolism, providing insights into adaptations to the cold and highly seasonal Antarctic environment. Population-level genome re-sequencing from four geographical sites around the Antarctic continent reveals no clear population structure but highlights natural selection associated with environmental variables. An apparent drastic reduction in krill population size 10 mya and a subsequent rebound 100 thousand years ago coincides with climate change events. Our findings uncover the genomic basis of Antarctic krill adaptations to the Southern Ocean and provide valuable resources for future Antarctic research. [Display omitted] • Assembly of the 48.01 Gb chromosome-level Antarctic krill genome • Extensive repeat expansions contributed to the giant Antarctic krill genome • Genetic adaptations to extreme variability of the Antarctic environment • Population analysis reveals no clear geographic differentiation in Antarctic krill The giant and highly repetitive Antarctic krill genome reveals environmental adaptations and population dynamics of Earth's most abundant wild animal. [ABSTRACT FROM AUTHOR]