He was the only son of Boris Kambulatovich Cherkassky and Marfa Nikitichna Romanova, a sister of Patriarch Filaret.
In 1599 he was arrested together with other prominent members of the Romanovs' party, and was exiled in 1601, but returned to Moscow in 1602.
After Mikhail Romanov was elected to become Tsar of Muscovy in 1613, Ivan Cherkassky was made a boyar.
A contemporary in 1634 wrote that Ivan Cherkassky managed affairs competently and didn't allow bureaucratic red tape to interfere with potential petitioners.
Cherkassky was married to Evdokia Vasilievna Morozova, a cousin of Boris Morozov.