Slotkin's professional experience included working for the Central Intelligence Agency as a political analyst (2003–2004) and intelligence briefer (2004–2005).
 From 2005 to 2006, she was a senior assistant on the staff of the Director of National Intelligence.
 She was the leader of a CIA assessment team in Iraq from 2006 to 2007 and the National Security Council staff's director for Iraq policy from 2007 to 2009.

From 2009 to 2011, Slotkin was a senior advisor on Iraq policy at the U.S. State Department, and in 2011 she joined the staff of the Under Secretary of Defense for Policy as an adviser on Middle East policy.
 In 2012, Slotkin became chief of staff for the Assistant Secretary of Defense for Policy, and later that year she was appointed Principal Deputy Assistant Secretary of Defense for Policy.
 Slotkin was appointed Principal Deputy Under Secretary of Defense for Policy in 2013, and in 2014 she was appointed as Principal Deputy Assistant Secretary of Defense for International Security Affairs.
 From 2015 to 2017, Slotkin was acting Assistant Secretary of Defense for International Security Affairs.

After leaving the Defense Department in January 2017, Slotkin moved back to her family's farm in Holly, where she owned and operated Pinpoint Consulting.

Since 2019, she has also been serving on the Transatlantic Task Force of the German Marshall Fund and the Bundeskanzler-Helmut-Schmidt-Stiftung (BKHS), co-chaired by Karen Donfried and Wolfgang Ischinger.
Slotkin's professional experience included working for the Central Intelligence Agency as a political analyst (2003–2004) and intelligence briefer (2004–2005).  From 2005 to 2006, she was a senior assistant on the staff of the Director of National Intelligence.  She was the leader of a CIA assessment team in Iraq from 2006 to 2007 and the National Security Council staff's director for Iraq policy from 2007 to 2009.
From 2009 to 2011, Slotkin was a senior advisor on Iraq policy at the U.S. State Department, and in 2011 she joined the staff of the Under Secretary of Defense for Policy as an adviser on Middle East policy.  In 2012, Slotkin became chief of staff for the Assistant Secretary of Defense for Policy, and later that year she was appointed Principal Deputy Assistant Secretary of Defense for Policy.  Slotkin was appointed Principal Deputy Under Secretary of Defense for Policy in 2013, and in 2014 she was appointed as Principal Deputy Assistant Secretary of Defense for International Security Affairs.  From 2015 to 2017, Slotkin was acting Assistant Secretary of Defense for International Security Affairs.
After leaving the Defense Department in January 2017, Slotkin moved back to her family's farm in Holly, where she owned and operated Pinpoint Consulting.
Since 2019, she has also been serving on the Transatlantic Task Force of the German Marshall Fund and the Bundeskanzler-Helmut-Schmidt-Stiftung (BKHS), co-chaired by Karen Donfried and Wolfgang Ischinger.
Elissa Slotkin