The ~150‐km‐wide dextral Marlborough Fault System and adjacent Kaikōura Mountains accommodate oblique convergence between the Pacific and Australian plates at the NE end of the South Island, New Zealand. Low‐temperature thermochronology from this region places new limits on the timing and style of Marlborough faulting and mountain building. We sampled rocks for apatite and zircon (U‐Th/He) and apatite fission track dating from a range of elevations spanning ~2 km within the Kaikōura Ranges, which stand high above the active Marlborough dextral faults. The data reveal Miocene cooling localized to hanging wall rocks, first along the Clarence Fault in the Inland Kaikōura Range, then along the Jordan Thrust in the Seaward Kaikōura Range, followed by widespread, rapid cooling reflected in all samples across the study area starting at ~5 Ma. Our results suggest that topographic relief in this region predates the onset of dextral faulting and that portions of the Marlborough Faults were once thrust faults that coincided with the early development of the transpressive plate boundary. We relate Pliocene to present rapid exhumation across the field site, including at low‐elevation sample sites in Marlborough Fault foot walls, to seaward translation and overthrusting of crust atop the downgoing slab by dextral Marlborough Fault motion. Our results show that spatial and temporal patterns in exhumation reflect a complex and evolving deformation field in the Marlborough Fault System over the past ~25 million years of Kaikōura orogeny.