The ability of cancer cells to alter their identity, known as lineage plasticity, is crucial for tumor progression and therapy resistance. In lung adenocarcinoma (LUAD), tumor progression is characterized by a gradual loss of lineage fidelity and the emergence of non-pulmonary identity programs. This can lead to hybrid-identity (hybrid-ID) states in which developmentally incompatible identity programs are co-activated within individual cells. However, the molecular mechanisms underlying these identity shifts remain incompletely understood. Here, we identify the gastrointestinal (GI) transcriptional regulator HNF4α as a critical driver of tumor growth and proliferation in KRAS-driven LUAD. In LUAD cells that express the lung lineage specifier NKX2-1, HNF4α can induce a GI/liver-like state by directly binding and activating its canonical targets. HNF4α also forms an aberrant protein complex with NKX2-1, which disrupts NKX2-1 localization and dampens pulmonary identity within hybrid-ID LUAD. Sustained signaling through the RAS/MEK pathway is critical for maintaining the hybrid-ID state. Moreover, RAS/MEK inhibition augments NKX2-1 chromatin binding at pulmonary-specific genes and induces resistance-associated pulmonary signatures. Finally, we demonstrate that HNF4α depletion enhances sensitivity to pharmacologic KRAS G12D inhibition. Collectively, our data show that co-expression of opposing lineage specifiers leads to a hybrid identity state that can drive tumor progression and dictate response to targeted therapy in LUAD.