This article discusses the origins of the central role of national security in Israeli foreign policy and analyses its implications for the relationship between Israel’s Office of the Prime Minister (PMO) and the Ministry of Foreign Affairs (MFA). The research focuses on the changing nature of this relationship between Israel’s PMO and MFA during the last three consecutive Netanyahu administrations from 2009 to 2018, and the reflection of those dynamics on Israel’s bilateral relations with the United States of America, Israel’s most important strategic ally. The author argues that the Israeli MFA has faced a rapid decline in its foreign policy competences and influence in the analysed period of 2009–2018. Moreover, this process has accelerated significantly since 2015 when Netanyahu decided to hold simultaneously a portfolio of Prime Minister as well as Minister of Foreign Affairs. Proposed reasons for the decline of the Israel’s MFA are enumerated.