A large proportion of plant carbon flow passes through the shikimate pathway to phenylalanine, which serves as a precursor for numerous secondary metabolites. To identify new regulatory mechanisms affecting phenylalanine metabolism, we isolated Arabidopsis thaliana mutants that are resistant to the phytotoxic amino acid m‐tyrosine, a structural analog of phenylalanine. Map‐based cloning identified adt2‐1D, a dominant point mutation causing a predicted serine to alanine change in the regulatory domain of ADT2 (arogenate dehydratase 2). Relaxed feedback inhibition and increased expression of the mutant enzyme caused up to 160‐fold higher accumulation of free phenylalanine in rosette leaves, as well as altered accumulation of several other primary and secondary metabolites. In particular, abundance of 2‐phenylethylglucosinolate, which is normally almost undetectable in leaves of the A. thaliana Columbia‐0 accession, is increased more than 30‐fold. Other observed phenotypes of the adt2‐1D mutant include abnormal leaf development, resistance to 5‐methyltryptophan, reduced growth of the generalist lepidopteran herbivore Trichoplusia ni (cabbage looper) and increased salt tolerance.