Increasing evidence suggests that long non-coding RNAs (lncRNAs) are involved in the regulation of plant tolerance to varying abiotic stresses. A large number of lncRNAs that are responsive to abiotic stress have been identified in plants; however, the mechanisms underlying the regulation of plant responses to abiotic stress by lncRNAs are largely unclear. Here, we functionally characterized a salt stress-responsive lncRNA derived from the leguminous model plant M. truncatula, referred to as MtCIR1, by expressing MtCIR1 in Arabidopsis thaliana in which no such homologous sequence was observed. Expression of MtCIR1 rendered seed germination more sensitive to salt stress by enhanced accumulation of abscisic acid (ABA) due to suppressing the expression of the ABA catabolic enzyme CYP707A2. Expression of MtCIR1 also suppressed the expression of genes associated with ABA receptors and signaling. The ABA-responsive gene AtPGIP2 that was involved in degradation of cell wall during seed germination was up-regulated by expressing MtCIR1. On the other hand, expression of MtCIR1 in Arabidopsis thaliana enhanced foliar Na+ accumulation by down-regulating genes encoding Na+ transporters, thus rendering the transgenic plants more sensitive to salt stress. These results demonstrate that the M. truncatula lncRNA MtCIR1 negatively regulates salt stress response by targeting ABA metabolism and signaling during seed germination and foliar Na+ accumulation by affecting Na+ transport under salt stress during seedling growth. These novel findings would advance our knowledge on the regulatory roles of lncRNAs in response of plants to salt stress.