Phenomics-in-depth phenotyping at the whole-organism scale-holds promise to enhance our fundamental understanding of genes and genomic variation, yet methods in vertebrates are limited. Here, we demonstrate rapid whole-body profiling of hundreds of traits in the axial skeleton of adult zebrafish. We show the potential for vertebral patterns to confer heightened sensitivity, with similar specificity, in discriminating mutant populations compared to analyzing individual vertebrae in isolation, even when the latter is performed at higher resolution. We identify phenotypes associated with human brittle bone disease and thyroid stimulating hormone receptor hyperactivity. Finally, we develop allometric models and show their potential to discriminate mutant phenotypes masked by growth alterations in growth. Our studies demonstrate virtues of whole-body phenomic pattern analysis in a single organ system. The high sensitivity may increase productivity in genetic screens, and facilitate the study genetic variants of smaller effect size, such as those that underlie complex diseases.