Quantifying the contribution of habitat dynamics relative to intrinsic population processes in regulating species persistence remains an ongoing challenge in ecological and applied conservation. Understanding these drivers and their relationship is essential for managing habitat‐dependent species, especially those that specialize in transitional habitats. Limitations in the ability of natural disturbance to mediate transitional habitat dynamics have resulted in a decline in early‐ and mid‐successional vegetation structure and prompted the need for aggressive habitat management to replace natural perturbations and increase habitat structural complexity. We describe a collaborative effort with a group of independent land managers to design an adaptive management program for restoring an imperiled ecosystem and recovering declining populations of an endemic habitat specialist. We developed a set of integrated, hierarchical models to estimate management‐mediated transition rates among vegetation classes in two dominant scrub communities and the species response (local colonization and extinction probabilities) as a function of habitat state. Models were fit using a long‐term data set of habitat and occupancy observations from 361 Florida scrub‐jay territories across two Florida counties. Occupancy model results correspond closely to previous approaches of estimating differential survival and reproductive success associated with habitat conditions, with highest colonization and lowest extinction rates estimated for those habitat states found to have the highest rates of survival and reproduction. In addition to offering an innovative approach for jointly modeling habitat and species population dynamics, the program we describe will also be of interest from a management perspective by providing guidance for developing collaborative, adaptive management frameworks from the ground up. We engaged land managers via workshops to specify objectives and desired state‐variable conditions, identify management alternatives, and elicit consensus opinions on model parameters. Treating expert opinions as pseudo‐observations to define Dirichlet priors allowed us to make use of existing management knowledge. Formal learning was then accumulated by updating transition probability estimates as management activities were implemented over the study period. We believe this adaptive management framework provides a useful approach for increasing our understanding of complex ecological relationships and hope that it will be adopted by others who have interest in informing management and conservation efforts.