High soil salinity is one of the most important environmental stressors, and is an increasing concern under the alarmingly global climate uncertainties. Salinity affects the growth and productivity of food crops, including rice, and ultimately threatens global food security and sustainability. Conventional breeding efforts to develop salt tolerant rice varieties utilizing its primary gene pool have resulted in limited success due to the mutligenic inheritance of salt tolerance traits. On the other hand, Porteresia coarctata, the only halophyte wild rice, offers tremendous opportunities to improve salt tolerance in rice. However, reports on the characterization of its rich genetic resources are scanty. The present study was undertaken to functionally identify salt responsive genes of P. coarctata in Arabidopsis model using a cDNA overexpression (COX) strategy. COX-mediated hunting of transgenic Arabidopsis expressing a cDNA library of P. coarctata under control of a maize ubiquitin promoter identified 12 candidates that were involved in salt tolerance for seed germination, and seedling and reproductive growth. Of these, four genes coding for a metallothionein, a ribosomal protein, a photosystem II 10 kDa protein, and a ferredoxin:thioredoxin reductase conferred enhanced salt tolerance phenotypes, such as better root and shoot growth, and tissue tolerance by maintaining higher relative water content, membrane stability and protecting cells from reactive oxygen species. These genes could be ideal candidates for improving salt tolerance in rice; however, further studies are needed to ascertain their direct functional relevance in salt tolerance mechanisms.