The eco-evolutionary tradeoff between microbial mitigation of carbon limitation and maintenance of functional traits in saline soils, a habitat rapidly expanding in extent under climate change, represents a significant knowledge gap in predicting future soil health and ecological function. Through shotgun metagenomic sequencing of coastal soils along a salinity gradient, we show contrasting eco-evolutionary directions of soil bacteria and archaea that manifest in changes to genome size and functional potential of the soil microbiome with increasing saline stress. Bacteria exhibited reduced genome sizes associated with a depletion of core metabolic genes in response to salinity, while archaea displayed larger genomes and an enrichment of salt-resistance, core metabolic genes, and especially an enhanced capacity for carbon acquisition in saline soils. This suggests that bacteria conserve energy through genome streamlining when facing salt stress, while archaea invest in carbon acquisition pathways to broaden their resource usage. These findings suggest divergent patterns in eco-evolutionary adaptations to soil saline stress amongst microbial clades and serve as a foundation for understanding the response of soil microbiomes to escalating climate change.