He joined the United States Foreign Service in 1972 and has served in Jerusalem, Budapest, Rome, Moscow, Vilnius, Tbilisi, and Kyiv.

[citation needed] Until his appointment as ambassador to Georgia, he was the deputy Assistant Secretary of State for European Affairs since July 6, 2004.

Tefft also served as International Affairs Advisor (Deputy Commandant) of the National War College in Washington, D.C. From 2000 to 2003, he was the United States Ambassador to Lithuania.

Strained relations with Russia over pro-separatist activity in eastern Ukraine, the country's annexation of Crimea, and the alleged shooting down of a commercial airliner, prompted senators to finally approve the nomination.

[11] In 2016, the Russian governor of the Samara Oblast, Nikolay Merkushkin, advised AvtoVAZagregat employees for help in paying wages and appeals to US Ambassador John Tefft.