Hill worked in the research department at the John F. Kennedy School of Government from 1991 to 1999, and at the National Intelligence Council as a national intelligence analyst of Russia and Eurasia from 2006 to 2009.
In 2017, she took a leave of absence from the Brookings Institution, where she was director for the Center on the United States and Europe, while also on the National Security Council.
Hill is a member of the Council on Foreign Relations and the board of trustees of the Eurasia Foundation.

In 1999, Hill was director of Harvard University's Strengthening Democratic Institutions project.

Hill was an intelligence analyst under Presidents George W. Bush and Barack Obama from 2006 to 2009.
She was appointed, in the first quarter of 2017, by President Donald Trump as Deputy Assistant to the President and Senior Director for European and Russian Affairs on his National Security Council staff.

Hill had been due to leave the White House to return to Brookings in April 2019.
She developed a close working relationship with National Security Advisor John Bolton, and at Bolton's request Hill agreed to stay on until mid July, when Tim Morrison would replace her.
As planned, Hill left the White House on July 15th, ten days before the Trump-Zelensky phone call.
Hill has subsequently spoken of the difficulty of maintaining a consistent US-Russia policy under President Trump, a result of the clash of her "hawkish" view on Russia and Trump's intermittently warm and welcoming approach, and of the difficulty of ascertaining what Trump and Putin discussed in private meetings.
She experienced hostility from Republicans, including Connie Mack who described Hill as a "George Soros mole infiltrating the national-security apparatus".
Hill worked in the research department at the John F. Kennedy School of Government from 1991 to 1999, and at the National Intelligence Council as a national intelligence analyst of Russia and Eurasia from 2006 to 2009. In 2017, she took a leave of absence from the Brookings Institution, where she was director for the Center on the United States and Europe, while also on the National Security Council. Hill is a member of the Council on Foreign Relations and the board of trustees of the Eurasia Foundation.
In 1999, Hill was director of Harvard University's Strengthening Democratic Institutions project.
Hill was an intelligence analyst under Presidents George W. Bush and Barack Obama from 2006 to 2009. She was appointed, in the first quarter of 2017, by President Donald Trump as Deputy Assistant to the President and Senior Director for European and Russian Affairs on his National Security Council staff. 
Hill had been due to leave the White House to return to Brookings in April 2019. She developed a close working relationship with National Security Advisor John Bolton, and at Bolton's request Hill agreed to stay on until mid July, when Tim Morrison would replace her. As planned, Hill left the White House on July 15th, ten days before the Trump-Zelensky phone call. Hill has subsequently spoken of the difficulty of maintaining a consistent US-Russia policy under President Trump, a result of the clash of her "hawkish" view on Russia and Trump's intermittently warm and welcoming approach, and of the difficulty of ascertaining what Trump and Putin discussed in private meetings. She experienced hostility from Republicans, including Connie Mack who described Hill as a "George Soros mole infiltrating the national-security apparatus".
Fiona Hill (presidential advisor)