Clitoria ternatea L. (Fabaceae) flowers are used widely in traditional medicine and are rich in anthocyanins. The methanolic extract of this flower was screened for phytochemical classes, profiled by GC-MS, and tested by MTT assay against HeLa, MCF-7, and A549 cells. Ten GC-MS-identified compounds were carried forward for ADMET prediction (ADMETlab 3.0) and molecular docking (AutoDock Vina) against six targets: EGFR (1M17), estrogen receptor α (3ERT), MDM2 (4HFZ), a Bcl-2/Bcl-xL chimera (2W3L), tubulin at the colchicine site (1SA0), and KRAS G12S (7TLG). Protein–ligand interactions were profiled with PLIP. The extract reduced viability in a concentration-dependent manner in all three lines, with IC50 values of 66.94 µg/mL (HeLa), 146.48 µg/mL (MCF-7), and 372.32 µg/mL (A549). HeLa cells were the most sensitive and A549 was the least sensitive cell line. Palmitic acid had the strongest support of evidence: published caspase-3-mediated cytotoxicity, the lowest predicted mutagenicity of the ten compounds, and salt-bridge interactions at two of the six targets. DDMP built the most specific hydrogen-bond network, at EGFR, though its predicted mutagenicity and carcinogenicity were both elevated. Overall, the extract shows cell-line-dependent cytotoxicity.