On Jun 19, 2009, Cousin was nominated by President Barack Obama to become United States Ambassador to the United Nations Agencies for Food and Agriculture, serving in Rome, Italy. She was confirmed by the United States Senate on August 7, 2009, and sworn in as Ambassador on August 17, 2009. There she is chief of the United States Mission to the UN Agencies in Rome and is part of the "Tri-Mission Community" that also includes the United States Ambassador to Italy and the United States Ambassador to the Holy See.
In January 2012, the U.S. State Department announced that Cousin would become Executive Director of the UN World Food Programme, succeeding Josette Sheeran when the latter's term expired in April 2012. Cousin was supported in a quote made by U.S. Secretary of State Hillary Rodham Clinton in reference to her appointment stating, "... [Cousin] has been central to designing and implementing our country's food security policies. I am confident that she will continue to be a powerful voice in the global fight against hunger and lend her energy, optimism and experience to the World Food Programme." Indeed, Cousin received the nomination after the U.S. opposed another term for Sheeran, who had been appointed by the George W. Bush administration.
Ertharin Cousin began her tenure as the twelfth Executive Director on April 5, 2012. In taking the position, she stated that she fully supported the WFP's transition from food aid to food assistance, saying "I think that debate is over. That WFP is a food assistance organization, with the right tools and those tools include food aid. But also cash and vouchers and all the other things we have on the table."