Estuaries, characterized by rapid and drastic salinity fluctuations, are transitional habitats between marine and freshwater ecosystems, representing an evolutionary barrier to organisms crossing this divide. However, repeated, bidirectional breaches across diverse lineages challenge the classical 'Rubicon' paradigm. Here, by integrating physiological assays, comparative genomics, and transcriptomics of a representative diatom lineage spanning the full salinity gradient, we elucidate how genomic and transcriptomic dynamics drive adaptive genomic streamlining across habitat transitions. We demonstrate two distinct evolutionary trajectories: lineage-specific gain and loss of adaptive repertoires, and targeted expansion of functional pathways. As evolutionary stepping stones, euryhaline estuarine generalists maintained high genomic versatility, while specialized freshwater and marine lineages achieved niche-specific adaptation through lineage-specific innovations and differential genomic streamlining. This study provides insights into how aquatic organisms balance genomic conservation and innovation to adapt to diverse salinity niches, offering a predictive framework for assessing the adaptive potential and evolutionary trajectories of primary producers under an intensifying global hydrological cycle.
 

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