Although sea lamprey (Petromyzon marinus) in the Laurentian Great Lakes have been studied intensively for more than 70 years, many questions remain about their complex life cycle. One of the least understood portions is the post-metamorphic stage (hereafter pre-feeding juvenile, PFJ) that occurs prior to parasitic feeding. PFJ must emerge from stream sediments and migrate downstream into nearshore feeding areas. Key uncertainties include the internal and exogenous triggers that regulate the timing and duration of the migration, and the mechanisms the animal uses to navigate, avoid predators, and locate their first host. However, many of these factors may vary predictably among natal streams in response to stable geomorphological and hydraulic characteristics that regulate the timing of movements (e.g., flood phenology), energetic costs (e.g., stream length), and risk (e.g., predator density). An improved understanding of the PFJ stage presents two opportunities to improve the success of sea lamprey control: (1) identification of streams where natural mortality during the PFJ stage is high, allowing for the reallocation of larval control to streams more likely to produce successful parasites, and (2) removal or killing of PFJs in streams where natural mortality is low. Either approach represents an opportunity to limit parasitic damage to valuable fish stocks. Here, we review the state of knowledge of the PFJ stage and identify critical knowledge gaps that, if addressed, could facilitate sea lamprey assessment and control by exploiting the behavior of PFJ as they outmigrate from streams in search of their first meal.