Previously to her position at the Defense Department, she was a senior fellow at the American Security Project, where she focused on stability and special operations, nonproliferation and East Asia–United States relations policy. In 2008, she served as executive director of the congressionally mandated Commission on the Prevention of Weapons of Mass Destruction Proliferation and Terrorism, which published its report World at Risk, in November 2008. From April 2001 to April 2008, she served as a professional staff member of the Senate Armed Services Committee. Her issue areas included foreign and defense policy in Asia Pacific, Western Hemisphere, Special Operations Command, foreign military assistance, peace and stability operations, the military effort to combat terrorism, counternarcotics programs, homeland defense, and export control policy. Prior to assuming that position she served for four years on the faculty of the U.S. Marine Corps Command and Staff College, Marine Corps University as assistant professor and then associate professor of international relations. She served in Bosnia for five months as a human rights officer for the Organization for Security and Cooperation in Europe during 1996, and as an election supervisor in 1997. Farkas is a member of the Council on Foreign Relations, International Institute for Security Studies, and Women in International Security Studies and is on the advisory board for the Harold Rosenthal Fellowship in International Relations and the Aspen Institute Socrates Program. In 2005 she served on a Council of Foreign Relations task force chaired by Samuel R. Berger and Brent Scowcroft that produced a monograph . In 2009 she became a member of the Center for National Policy's Future Forces advisory group. She is also a blogger for National Journal. Farkas's publications include journal articles and opinion pieces in The Washington Post and Los Angeles Times on issues including Balkan peace operations and military readiness. She is also the author of the 2003 book, Fractured States and U.S. Foreign Policy: Iraq, Ethiopia, and Bosnia in the 1990s. In March 2017, conservative news media and White House spokesperson Sean Spicer placed Farkas at the center of the controversy surrounding President Donald Trump's team and their alleged ties with Russia. In an appearance on MSNBC on March 2, Farkas had commented on her role in the efforts to preserve intelligence on Trump’s team in the waning days of the Obama administration, stating, “I was urging my former colleagues and, frankly speaking, the people on the Hill... get as much information as you can," Farkas said, adding that her big fear was "if found out how we knew what we knew about their... the Trump staff dealing with Russians – that they would try to compromise those sources and methods, meaning we no longer have access to that intelligence.” Later, when questioned under oath in front of the House Permanent Select Committee on Intelligence on June 26, 2017, as part of the committee’s investigation into Russian interference in the 2016 presidential election, then Representative Trey Gowdy asked Farkas, “All right. So if you had to do this interview all over again, you would say, I know nothing other than what your viewers are reading in the paper and watching on television, and I have no evidence that the Trump campaign colluded, conspired, or coordinated with the Russians?” Farkas’s response was, “Correct.” Gowdy then asked, “That’s what you would say if you were being interviewed now?” Farkas stated, “Yeah.”
Congressional campaign
Farkas moved back to her childhood home in Chappaqua, New York to run as a Democrat to succeed longtime Representative Nita Lowey in New York's 17th congressional district. Despite endorsements from major Democratic figures such as former Secretary of State John Kerry, Farkas finished in third place in the crowded Democratic primary with 15.6% of the vote.