Plants employ several strategies to maintain cellular ion homeostasis under salinity stress, including mediating ion fluxes by transmembrane transport proteins and adjusting osmotic pressure by accumulating osmolytes. The HKT (high-affinity potassium transporter) gene family comprises Na+ and Na+/K+ transporters in diverse plant species, with HKT1;1 as the only member in Arabidopsis thaliana. Cell-type-specific overexpression of AtHKT1;1 has been shown to prevent shoot Na+ overaccumulation under salinity stress. Here, we analyzed a broad range of metabolites and elements in shoots and roots of different AtHKT1;1 genotypes and their parental strains before and after salinity stress, revealing a reciprocal relationship of metabolite differences between an AtHKT1;1 knockout line (hkt1;1) and the AtHKT1;1 overexpressing lines (E2586 UASGAL4:HKT1;1 and J2731*UASGAL4:HKT1;1). Although levels of root sugars were increased after salt stress in both AtHKT1;1 overexpressing lines, E2586 UASGAL4:HKT1;1 showed higher accumulation of the osmoprotectants trehalose, gentiobiose, and melibiose, whereas J2731*UASGAL4:HKT1;1 showed higher levels of sucrose and raffinose, compared with their parental lines, respectively. In contrast, the knockout line hkt1;1 showed strong increases in the levels of the tricarboxylic acid (TCA) cycle intermediates in the shoots after salt treatment. This coincided with a significant depletion of sugars, suggesting that there is an increased rate of carbon influx into the TCA cycle at a constant rate of C-efflux from the cycle, which might be needed to support plant survival during salt stress. Using correlation analysis, we identified associations between the Na+ content and several sugars, suggesting that regulation of sugar metabolism is important in plant responses to salinity stress.