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Cell Painting images offer valuable insights into a cell's state and enable many biological applications, but publicly available arrayed datasets only include hundreds of genes perturbed. The JUMP Cell Painting Consortium perturbed roughly 75% of the protein-coding genome in human U-2 OS cells, generating a rich resource of single-cell images and extracted features. These profiles capture the phenotypic impacts of perturbing 15,243 human genes, including overexpressing 12,609 genes (using open reading frames) and knocking out 7,975 genes (using CRISPR-Cas9). Here we mitigated technical artifacts by rigorously evaluating data processing options and validated the dataset's robustness and biological relevance. Analysis of phenotypic profiles revealed previously undiscovered gene clusters and functional relationships, including those associated with mitochondrial function, cancer and neural processes. The JUMP Cell Painting genetic dataset is a valuable resource for exploring gene relationships and uncovering previously unknown functions.