Asian cultivated rice shows allelic variation in sodium transporter, OsHKT1;5, correlating with shoot sodium exclusion (salinity tolerance). These changes map to intra/extracellularly-oriented loops that occur between four transmembrane-P loop-transmembrane (MPM) motifs in OsHKT1;5. HKT1;5 sequences from more recently evolved Oryza species (O. sativa/O. officinalis complex species) contain two expansions that involve two intracellularly oriented loops/helical regions between MPM domains, potentially governing transport characteristics, while more ancestral HKT1;5 sequences have shorter intracellular loops. We compared homology models for homoeologous OcHKT1;5-K and OcHKT1;5-L from halophytic O. coarctata to identify complementary amino acid residues in OcHKT1;5-L that potentially enhance affinity for Na+. Using haplotyping, we showed that Asian cultivated rice accessions only have a fraction of HKT1;5 diversity available in progenitor wild rice species (O. nivara and O. rufipogon). Progenitor HKT1;5 haplotypes can thus be used as novel potential donors for enhancing cultivated rice salinity tolerance. Within Asian rice accessions, 10 non-synonymous HKT1;5 haplotypic groups occur. More HKT1;5 haplotypic diversities occur in cultivated indica gene pool compared to japonica. Predominant Haplotypes 2 and 10 occur in mutually exclusive japonica and indica groups, corresponding to haplotypes in O. sativa salt-sensitive and salt-tolerant landraces, respectively. This distinct haplotype partitioning may have originated in separate ancestral gene pools of indica and japonica, or from different haplotypes selected during domestication. Predominance of specific HKT1;5 haplotypes within the 3000 rice dataset may relate to eco-physiological fitness in specific geo-climatic and/or edaphic contexts.