Iran’s experience with terrorism is not new. The state has both supported and directed terrorist organizations and attacks, and has been the victim of terrorism from groups within its borders. This chapter examines the shifts in the Iranian experience of post-9/11 terrorism. This chapter argues that despite regional and international opposition to Iranian foreign policy by proxy, Iranian involvement in the fight against ISIS has been fundamental to the endeavour to undermine the group. However, with the prospect of ISIS being overpowered in the Middle East, any potential cooperation on regional objectives between Iran and the US will likely subside. First, the chapter examines the history of Iranian involvement in terrorism since the Iranian Revolution. While initially a vital part of its foreign policy, towards the early 2000s Iranian support for terror organizations declined significantly. Second, the chapter explores the post-9/11 environment and its effect on Iranian regional engagement. Although Iran was supportive of the US in the invasion of Afghanistan and Iraq, and an important ally in attempts to dismantle the Taliban regime and al-Qaeda, the US decision to label Iran as part of the ‘axis of evil’ undermined any positive moves by Iran to normalize its foreign policy. Instead, towards the end of that decade, Iran began to increase its direct and indirect involvement in terrorism to counter US and Israeli power in the Middle East. Finally, the chapter examines the rise of Islamic State and the shifting geopolitical realities Iran currently contends with, illustrating how goals of both Iran and the United States did overlap in terms of defeating ISIS.