He joined him in the War of the Succession of Stettin with the Pomeranian dukes, until Frederick resigned in 1470 and was succeeded by John's father, who in 1473 appointed him regent of the Brandenburg lands.

On 25 August 1476 in Berlin John married Margaret of Wettin, a daughter of Landgrave William III of Thuringia with Anne, Duchess of Luxembourg.

Their children were: John succeeded his father as elector in 1486, while the Franconian possessions of the Hohenzollern dynasty passed to his younger brothers Frederick I and Siegmund.

He decreed that the Stadtschloss in Berlin, erected at the behest of his uncle Frederick II, should serve as the permanent residence of the Brandenburg electors, the beginning of the city's history as a state capital.

In 1490 John was able to purchase the former Lusatian territory around Zossen, acknowledged by the Bohemian king Vladislaus II, and maintained the succession claims of the Hohenzollern dynasty to the Pomeranian lands held by the House of Griffins.