Soil salinity severely affects plant growth and agricultural productivity. AtbZIP24 encodes a bZIP transcription factor that is induced by salt stress in Arabidopsis thaliana but suppressed in the salt-tolerant relative Lobularia maritima. Transcriptional repression of AtbZIP24 using RNA interference improved salt tolerance in A. thaliana. Under non-stress growth conditions, transgenic A. thaliana lines with decreased AtbZIP24 expression activated the expression of stress-inducible genes involved in cytoplasmic ion homeostasis and osmotic adjustment: the Na(+) transporter AtHKT1, the Na(+)/H(+) antiporter AtSOS1, the aquaporin AtPIP2.1, and a glutamine synthetase. In addition, candidate target genes of AtbZIP24 with functions in plant growth and development were identified such as an argonaute (AGO1)-related protein and cyclophilin AtCYP19. The salt tolerance in transgenic plants correlated with reduced Na(+) accumulation in leaves. In vivo interaction of AtbZIP24 as a homodimer was shown using fluorescence energy transfer (FRET) with cyan fluorescent protein (CFP) and yellow fluorescent protein (YFP) as fused FRET pairs. Translational fusion of AtbZIP24 with GFP showed subcellular localization of the protein in nucleus and cytoplasm in plants grown under control conditions whereas in response to salt stress AtbZIP24 was preferentially targeted to the nucleus. It is concluded that AtbZIP24 is an important regulator of salt stress response in plants. The modification of transcriptional control by regulatory transcription factors provides a useful strategy for improving salt tolerance in plants.