In July 1735, the resurgent Persian ruler Nader Shah Afshar invaded Kakheti and forced the Turks out of most of eastern Georgia.

In 1738, the Persian shah had to release Teimuraz to counter the Georgian opposition, and made him governor of Kakheti, while his son Erekle II campaigned with Nader in India.

As a reward, the shah abolished, in 1742, a heavy tribute laid upon Kakheti, and helped Teimuraz to subdue autonomous duchies of the Aragvi and the Ksani in 1743 and 1744 respectively.

For his service against the Ottomans and an anti-Persian revolt, in 1744, Teimuraz was confirmed by the shah as king of Kartli, and his son Erekle was given a Kakhetian crown, thus laying the ground for the eventual reunification of these Georgian kingdoms.

From 1749 to 1750, they checked several attempts of Persian pretenders to create their powerbase in the eastern Transcaucasia, and made the neighbouring khanates of Yerevan, Ganja, and Nakhichevan their tributaries.

Like several previous Georgian rulers, he hoped that the expanding Russian Empire would be the only protector for the Christians of Caucasus against the Ottoman and Persian aggressions.

He died suddenly in the Russian capital on January 8, 1762 (just a fortnight after Elizabeth of Russia incidentally), and was buried next to his father-in-law Vakhtang VI in the Cathedral of the Assumption, Astrakhan.