Efficient control of ion homeostasis and nitrogen (N) metabolism contributes to the salt tolerance in crops. However, limited information is available on the contribution of ion homeostasis and N metabolism regulation towards salt tolerance in sweet potato (Ipomoea batatas L.) cultivars at adventitious root stage. In this study, NaCl-induced ion homeostasis and N metabolism changes in adventitious roots of two different sweet potato cultivars were investigated. Salt tolerant cultivar (Xushu 22, Xu 22) exhibited better capacity controlling Na+, Cl−, K+ and Mg2+ homeostasis than the salt sensitive cultivar (Xushu Shi 5, Shi 5) under prolonged salinity condition. Net H+ efflux and plasma membrane H+-ATPase gene expression were significantly enhanced in NaCl-stressed Xu 22 roots but not in Shi 5 roots. Salt-upregulated PM H+-ATPase contributed to less K+ efflux in Xu 22 roots. NaCl stimulated Mg2+ uptake in Xu 22 roots under prolonged salinity, but promoted Mg2+ efflux in Shi 5 roots. In addition, NaCl significantly enhanced transcript abundance of genes related to vacuolar Na+ and Cl− sequestration in Xu 22 roots. In Xu 22 roots, NaCl triggered an obvious net NH4+ efflux, which caused a rapid increase of NH4+ concentration around the rhizosphere. Exogenous supply of NH4+ markedly inhibited Na+ influx and K+ efflux under salt shock condition. Moreover, a salt-enhanced NO3− net influx was also detected in mature Xu 22 root region and this process may contributes to the normal N assimilation in this cultivar under prolonged saline condition. Taken together, our results suggest that the better capacities of root K+ and Mg2+ retention, vacuolar Na+ and Cl− sequestration, transition of NH4+/NO3− transport and N assimilation maintenance contribute to the salt tolerance of Xu 22 at adventitious root stage. A model showing salt-adaptive mechanisms in salt-tolerant Xu 22 is proposed.