<p>Asgard archaea hold a pivotal position in the tree of life as the closest known relatives to eukaryotes and are therefore crucial for understanding eukaryogenesis. Earlier genomic analyses revealed that Asgard genomes are remarkably larger than those of other archaea and contain a significant number of genes seemingly acquired from bacteria. However, the precise contributions of horizontal gene transfer and gene duplication in shaping Asgard genomes remain largely unknown. Here, we present a comprehensive phylogenomic analysis to dissect the evolutionary dynamics of Asgard genomes, quantifying gene duplication, loss, and both inter- and intra-domain gene transfer events. Our findings reveal that gene transfer is widespread throughout Asgard evolution, predominantly affecting metabolic genes at the periphery of interaction networks. However, our analyses demonstrate that gene duplications, rather than horizontal gene transfers, are the primary drivers behind the increased genome sizes observed in Asgard archaea. This unique evolutionary signature in Asgard archaea—a blend of pervasive prokaryotic-like gene transfer alongside significant eukaryotic-like gene duplication—is consistent with their phylogenetic placement and offers novel insights into the genomic transitions that likely underpinned eukaryogenesis.</p>