His father died in 1573, when Johann was only three years old. Since at the time his older brother Frederick William I was also under age, the duchy of Saxe-Weimar (originally awarded to Johann) was governed by a regency. In 1586 his older brother reached adulthood and took full control of the duchy, including Weimar. However, he died in 1602 and the full duchy was inherited by Johann, because his nephews (the sons of his deceased brother) were under age.

Johann was more interested in natural sciences and art than politics, and therefore only against his will took over the regency of the duchy on behalf of his nephews. But when they demanded their own inheritance in 1603, he resisted their demands. Finally, Johann and his nephews made a treaty dividing the duchy: Altenburg was taken by the sons of Frederick William I, and Weimar-Jena was retained by Johann.

This line of Saxe-Altenburg became extinct in 1672, and all the inheritance passed to the line of Saxe-Weimar, Johann's descendants.

In Altenburg on 7 January 1593, Johann married Dorothea Maria of Anhalt (b. 2 July 1574 d. 18 July 1617). They had twelve children:

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