Recent molecular systematic research has indicated the need for a revised circumscription of generic boundaries in subtribe Castillejinae (tribe Pedicularideae, Orobanchaceae). Based on a well-resolved and well-supported phylogenetic hypothesis, we present a formal reclassification of the major lineages comprising the Castillejinae. Prior to this treatment, subtribe Castillejinae included Castilleja (ca. 190 spp.), Cordylanthus (18 spp.), Orthocarpus (9 spp.), Triphysaria (5 spp.), and the monotypic genera Clevelandia and Ophiocephalus. In the classification presented here, Orthocarpus and Triphysaria retain their current circumscriptions, Castilleja is expanded to include Clevelandia and Ophiocephalus, and Cordylanthus is split into three genera; a key to the genera as they are recognized here is provided. Two new combinations, Castilleja beldingii and Castilleja ophiocephala, are proposed within the expanded Castilleja. The concept of Coriylanthus is restricted to the 13 species formerly recognized as subg. Coriylanthus, while subg. Dicranostegia and subg. Hemistegia are elevated to genus level (Dicranostegia and Chloropyron, respectively). We resurrect the generic name Chloropyron for the halophytes previously recognized as subg. Hemistegia. Five new combinations are proposed for Chloropyron (Chloropyron maritimum subsp. canescens, Chloropyron maritimum subsp. palustre, Chloropyron molle subsp. hispidum, Chloropyron palmatum, and Chloropyron tecopense). In addition to the formal classification, we provide phylogenetic clade definitions for Castillejinae, each of the genera, and two additional clades that are not assigned formal ranks. Morphological characteristics used to recognize traditional groups are evaluated, and synapomorphies are discussed. Finally, the current infrageneric classifications for Castilleja and Coriylanthus are evaluated in light of the recent molecular phylogenetic analyses.