The Bruin Bay fault system defines the northwestern tectonic boundary of the Cook Inlet forearc basin for ∼450 km along the southern Alaskan forearc. The age, origin, and tectonic significance of the fault system are not well understood. We present field observations and a population of minor fault slip data (n = 296) collected within the Bruin Bay fault system from the Iniskin-Tuxedni region of the Cook Inlet. The minor faults cut Triassic–Paleogene strata and are subdivided into two kinematically distinct populations. Population A (n = 233, 79%) includes strike-slip and reverse faults that altogether record subhorizontal, southeast-trending tectonic shortening and bulk sinistral transpression. Population B (n = 63, 21%) includes strike-slip faults that are compatible with subhorizontal, northeast-trending shortening and southeast-trending extension and are younger. Gently deformed mafic and felsic dikes that intrude cataclasite within the Bruin Bay fault zone at two localities yield late Paleogene biotite (ca. 37 Ma), whole-rock (ca. 33 Ma), and plagioclase (ca. 31 Ma) 40Ar/39Ar ages. The ages of deformed strata and crosscutting dikes indicate that sinistral transpression (population A) occurred during the Paleogene prior to ca. 37 Ma, but some deformation persisted through at least the early Oligocene. Results place the Bruin Bay fault system in the Paleogene tectonic context of southern Alaska. We discuss several competing hypotheses to interpret the tectonic evolution of the fault system. We suggest that the majority of the Paleogene deformation likely occurred during either a spreading ridge subduction event or accretion of the Chugach–Prince William terrane to the southern Alaskan margin.