In the fall of 2014 the U.S. Department of Defense launched simultaneously the Defense Innovation Initiative and the Third Offset Strategy aimed at ensuring American military and technological superiority in the XXI century. However, the linkages between dynamics of innovation development and evolution of defense strategy would manifest itself in the past. This paper examines those linkages by focusing on the strategic determinants and dividends of several innovation breakthroughs using the methodological framework of synergetics. The author identifies three major milestones, each marking the beginning of a new stage in innovation development of the U.S. economy: 1958, late 1970s - early 1980s, and the fall of 2014. Each stage corresponds with a set of specific technologies and concepts of ensuring the American global military, technological and political leadership, the so called ‘offset strategies’. The paper focuses on the role of the Defense Advanced Research Projects Agency (DARPA) in the development of the U.S. national innovation system and the establishment of technological and conceptual foundations of deterrence strategy. The paper examines both the particularities of the DARPA research and development programs and its cooperation with other defense and academic institutions. The author emphasizes that it is a unique combination of flexibility and adaptability, interdisciplinary nature of each project, and special focus on the dual-use technologies, that has already helped DARPA to become an engine of the U.S. defense economy. The shape and the substance of the Third Offset Strategy, are also defined, in large part, by DARPA. The author concludes that the study of DARPA’s programs, which exemplify a dichotomous link between innovation development and deterrence strategy, could be instrumental in understanding the impact of innovative technologies on parameters of strategic stability.