Phosphorus (P) is a crucial macronutrient required for normal plant growth. Its effective uptake from the soil is a trait of agronomic importance. Natural variation in maize (339 accessions) root traits, namely root length and number of primary, seminal, and crown roots, root and shoot phosphate (Pi) contents, and root‐to‐shoot Pi translocation (root: shoot Pi) under normal (control, 40 ppm) and low phosphate (LP, 1 ppm) conditions, were used for genome‐wide association studies (GWAS). The Bayesian‐information and Linkage‐disequilibrium Iteratively Nested Keyway (BLINK) model of GWAS provided 23 single nucleotide polymorphisms (SNPs) and 12 relevant candidate genes putatively linked with root Pi, root: shoot Pi, and crown root number (CRN) under LP. The DNA‐protein interaction analysis of Zm00001d002842, Zm00001d002837, Zm00001d002843 for root Pi, and Zm00001d044312, Zm00001d045550, Zm00001d025915, Zm00001d044313, Zm00001d051842 for root: shoot Pi, and Zm00001d031561, Zm00001d001803, and Zm00001d001804 for CRN showed the presence of potential binding sites of key transcription factors like MYB62, bZIP11, ARF4, ARF7, ARF10 and ARF16 known for induction/suppression of phosphate starvation response (PHR). The in‐silico RNA‐seq analysis revealed up or down‐regulation of candidate genes along with key transcription factors of PHR, while Uniprot analysis provided genetic relatedness. Candidate genes that may play a role in P uptake and root‐to‐shoot Pi translocation under LP are proposed using common PHR signaling components like MYB62, ARF4, ARF7, ARF10, ARF16, and bZIP11 to induce changes in root growth in maize. Candidate genes may be used to improve low P tolerance in maize using the CRISPR strategy.