In 1939 the Roosevelt White House created a new agency with vast legal powers. The enormous Federal Security Agency (or FSA) soon held responsibility for matters involving social security, education, drug regulation, protection of the food supply, civil defense preparedness, supplying employees to war-related industries, facilitating the relocation of Japanese-Americans, anti-prostitution enforcement, and conducting biological weapons research. Although the FSA was disbanded in 1953, it engendered one of the most important American bureaucracies of the 20th century: the Department of Health, Education, and Welfare. Yet little is known about precisely how or why the FSA was created, why it pervasively mixed domestic administrative and national defense functions both before and after World War II, or what its creation wrought for the legal mandates entrusted to the agency. This paper investigates these questions. The analysis reveals how, on the eve of World War II, the White House sought to use the restructuring to achieve greater control over the agency’s many functions by building bureaucratic oversight capacity. It then used that control to promote a broader conception of security that held the prospect of more thoroughly protecting domestic programs important to the Administration. And by rendering ambiguous the distinction between domestic and national security functions, the Administration enlarged support for some of its signature programs at a time when the New Deal legislative coalition was eroding. In effect, the agency’s amalgam of legal functions came to epitomize the Administration’s ambitious conception of security, which became sufficiently elastic to encompass legal responsibilities now routinely segregated into domains involving social services, economic security, health regulation, and geostrategic national security. The creation of the FSA also appears to have fomented more subtle (intended and unintended) impacts on matters such as the organization of congressional committees overseeing the agency’s legal functions, and the prospects for bureaucratic autonomy among the agency and its sub-units. These dynamics illustrate the limitations inherent in theories of bureaucracy focusing exclusively on deliberately engineered organizational failure, purely symbolic position-taking, or the spontaneous development of internal routines and cultures. They also showcase the ambiguities inherent in the definition of security as a category of government responsibility. Presidential administrations and bureaucratic actors used that ambiguity to bolster political coalitions supporting social welfare and regulatory mandates; the recent spike of interest in homeland security may ultimately furnish similar opportunities to reshape domestic administrative and regulatory activities.