During WWII, he was a top member of the OSS, serving alone at the Berne station where he ran deep cover operations within the Reich and even helped in the failed bomb plot against Hitler. These secret Nazi connections were later exploited by him — along with ANGLETON, HELMS, and others — when secret deals placed Nazis like REINHARD GEHLEN and KLAUS BARBIE in important positions around the world.

In 1953 he became the 2nd DCI. Under his watch, the CIA became the covert action wing of the government, ostensibly under Presidential control. Under Dulles, coups were staged in Guatemala, Iran, Indonesia, Vietnam, and elsewhere. A massive global propaganda machine was created, and called "The Mighty Wurlitzer" by its commanders. In its darkest shadows, the Agency gave birth to the MK-ULTRA mind control program.

Fired by JFK after the Bay of Pigs disaster, Dulles later helped engineer his assassination and the subsequent cover-up, knowingly hiding key information from the Warren Commission, quashing important lines of investigation, and apparently even .