The genus Agalinis (commonly known as the “false foxgloves”) belonging to the family Orobanchaceae, is native to the Western Hemisphere. Approximately 40 species are distributed across temperate North America, and a large group is native to Missouri and the Midwestern United States. Twenty-one species of this genus warrant conservation measures. Our main aims were to understand the migration and diversification of temperate North American Agalinis, as well as focusing on the six species native to the state of Missouri. This study is the first to investigate the evolutionary diversification of this genus in temperate North America. Computer applications including BEAST (Bayesian evolutionary analysis sampling trees) and SDIVA (statistical dispersal vicariance analysis), and secondary calibrations from previous studies were implemented to understand the diversification timings and ancestral areas of this group. Our study points to southeastern United States as the center of diversity and place of origin of the Agalinis in temperate North America, from which they spread to the rest of the United States and even migrated to Canada, around the mid-late Miocene period. We were also able to trace the biogeography of the Missouri natives which diversified between the late Miocene and the Pleistocene period. It may be hypothesized that climatic shifts and increase in seasonality during the mid-late Miocene period was one of the primary causes leading to the migration and diversification of this genus throughout temperate North America.