He was the second but eldest surviving son of William, Duke of Saxe-Weimar, and Eleonore Dorothea of Anhalt-Dessau.
In 1672 John Ernest divided his possessions with his younger brothers.
Eventually, the partitioned lands, Saxe-Weimar, Saxe-Eisenach (1741) and Saxe-Jena (1690) were re-combined.
Like his father, John Ernest was particularly interested in the arts (see Fruitbearing Society).
Given his overriding interest in these pursuits, John Ernest entrusted the reigns of government to his chancellor.