On his death in 1440, his territories were again divided between his sons: the eldest, John the Alchemist had waived his right of primogeniture and succeeded his father in Kulmbach-Bayreuth, while the second, Frederick Irontooth, received the Brandenburg electorate.

After Albert's death in 1486 the Franconian principalities were finally partitioned according to his Dispositio Achillea disposition, passing to the younger sons of his second marriage with Anna of Saxony, Margrave Siegmund and his brother Frederick II.

While the Brandenburg electorate became the power base for the rising Hohenzollern dynasty, the Principality of Kulmbach-Bayreuth was held by Frederick's descendants, temporarily in personal union with Ansbach.

Margrave Frederick, ruling from 1735, and his wife Wilhelmine of Prussia, both patrons of arts and sciences, had the Bayreuth residence largely rebuilt in a distinct Baroque style (Markgrafenstil), including the erection of the Margravial Opera House finished in 1748.

On 2 December 1791, Charles Alexander signed a treaty with King Frederick William II of Prussia, whereby he ceded his principalities to the Prussian state against a lifelong annuity.

He married socialite Elizabeth Craven and retired to private life in England, while Bayreuth and Ansbach were governed by the Prussian minister Karl August von Hardenberg.

At the 1808 Congress of Erfurt, the French emperor Napoleon offered it for sale to the newly established Kingdom of Bavaria; it changed owners in 1810 against a payment of 15 million francs.