Using GWAS, 13 significant SNPs distributed on six of the seven Aegilops tauschii chromosomes (all but 5D) were identified, and several candidate P-deficiency-responsive genes were proposed from searches of public databases. Aegilops tauschii, the wheat (Triticum aestivum) D-genome progenitor, possesses numerous genes for stress resistance, including genes for tolerance of phosphorus (P) deficiency. Investigation of the genetic architecture of A. tauschii will help in developing P-deficiency-tolerant varieties of wheat. We evaluated nine traits in a population of 380 A. tauschii specimens under conditions with and without P application, and we performed genome-wide association studies for these traits using single nucleotide polymorphism (SNP) chips containing 7185 markers. Using a general linear model, we identified 119 SNPs that were significantly associated with all nine traits, and a mixed linear model revealed 18 SNPs associated with all traits. Both models detected 13 significant markers distributed on six of the seven A. tauschii chromosomes (all but 5D). Searches of public databases revealed several candidate/flanking genes related to P-deficiency tolerance. These genes were grouped in five categories by the types of proteins they encoded: defense response proteins, enzymes, promoters and transcription factors, storage proteins, or proteins triggered by P deficiency. The identified SNPs and genes contain essential information for cloning genes related to P-deficiency tolerance in A. tauschii and wheat, and they provide a foundation for breeding P-deficiency tolerant wheat cultivars.