Given the global rates of freshwater depletion and the lack of replenishment in many regions, the use of saline water as a primary source of irrigation for cropping will become increasingly important. Our group aims to domesticate an obligate halophyte, Salicornia spp., as an oilseed crop for arid environments and in the process, understand the underlying mechanisms of shoot sodium accumulation. De novo assembly of reference genomes for seven Salicornia species varying in ploidy and genome size was validated by chromosome painting of 5s and 45s rDNA loci and mapping of repetitive DNA using oligo painting FISH. Amplification of a TY3/Gypsy retrotransposon family was determined to contribute to the enlargement of Salicornia bigelovii (2138 Mb, 2n = 4x =36) relative to Salicornia europaea (580 Mb, 2n = 2x = 18). Untargeted membrane proteomics of Salicornia bigelovii led to the identification of a sodium transporter, SALT-OVERLY-SENSITIVE 1 (SOS1) on the vacuolar membrane and its localisation was confirmed in both N and C-terminal GFP fusions. Arabidopsis SOS1 was characterized to localise to the plasma membrane. Here, we suggest that the neofunctionalization of SOS1 in Salicornia spp. aids vacuolar sequestration of sodium. In addition, SbiSALTY protein, an ortholog of AtRGGA, was identified at the same density as ribosomes and the rough ER. NMR was used to confirm that SbiSALTY is an intrinsically disordered protein. We speculate that SbiSALTY binds to RNA-containing structures such as ribosomes at the region predicted to form coiled-coil, stabilizing or protecting them during salt stress.