The putative FASCICLIN-LIKE ARABINOGALACTAN PROTEIN 4 (At-FLA4) locus of Arabidopsis thaliana has previously been shown to be required for the normal growth of wild-type roots in response to moderately elevated salinity. However, the genetic and physiological pathway that connects At-FLA4 and normal root growth remains to be elucidated. The radial swelling phenotype of At-fla4 was modulated with growth regulators and their inhibitors. The relationship of At-FLA4 to abscisic acid (ABA) signalling was analysed by probing marker gene expression and the observation of the At-fla4 phenotype in combination with ABA signalling mutants. Application of ABA suppresses the non-redundant role of At-FLA4 in the salt response. At-FLA4 positively regulates the response to low ABA concentration in roots and is required for the normal expression of ABA- and abiotic stress-induced genes. The At-fla4 phenotype is enhanced in the At-abi4 background, while two genetic suppressors of ABA-induced gene expression are required for salt oversensitivity of At-fla4. Salt oversensitivity in At-fla4 is suppressed by the CYP707A inhibitor abscinazole E2B, and salt oversensitivity in At-fla4 roots is phenocopied by chemical inhibition of ABA biosynthesis. The predicted lipid-anchored glycoprotein At-FLA4 positively regulates cell wall biosynthesis and root growth by modulating ABA signalling.