The maize shoot apical meristem (SAM) comprises a small pool of stem cells that generate all the organs in the above ground plant. Mutational analyses have identified genetic networks regulating SAM function, although little is known about the genetic determinants of SAM morphological variation in natural populations. We utilized high-throughput image processing to capture rich variation in SAM size for a diverse panel of maize inbred varieties, wild teosinte isolates, and a domesticated maize x wild progenitor teosinte backcross population. Focusing on diverse maize inbred lines, we identified significant correlations between seedling SAM size and agronomically-important adult plant traits such as flowering time, stem size, and leaf node number. Combining SAM phenotype data with a 1.2-million-SNP dataset in a genome-wide association study (GWAS) revealed unexpected SAM morphology candidate genes. We further confirmed correlations between SAM morphology and trait-associated SNP (TAS) alleles of several GWAS-derived SAM candidate genes through in situ hybridization and cell number and size estimation via image segmentation. Our data illustrate that the microscopic seedling SAM is predictive of adult phenotypes and that SAM morphometric variation is associated with genes that were not previously predicted to regulate SAM size. In further exploration of natural variation of SAM shape and size, we implemented rapid and complex morphometric modeling approaches to quantify SAM morphology. Quantitative trait loci (QTL) mapping results suggest that a majority of genetically-attributable SAM shape and size variation can be captured by estimating the SAM as a paraboloid, which has several advantages for high-throughput phenotyping methods. Further application of this model to a broad sampling of evolutionarily-distant plant species suggests that a parabolic SAM may be a universal trait of plant meristems. Future investigations into the mechanisms that orchestrate parabolic SAM parameters may reveal additional correlations between SAM architecture and adult plant morphology that transcend phylogenetic determinants.