This Article examines the endurance of police localism amid the improbable growth of the FBI in the early twentieth century when the prospect of a centralized law enforcement agency was anathema to the ideals of American democracy. It argues that doctrinal accounts of federalism do not explain these paradoxical developments. By analyzing how the Bureau made itself indispensable to local police departments rather than encroaching on their turf, the Article elucidates an operational, or collaborative, federalism that not only enlarged the Bureau’s capacity and authority but also strengthened local autonomy at the expense of the states. Collaborative federalism is crucial for understanding why the police have gone for so long without meaningful state or federal oversight, with consequences still confronting the country today. This history highlights how structural impediments to institutional accountability have been set over time and also identifies a path not taken, but one that can still be pursued, to expand the states’ supervisory role over local police.