He resumed his rule of Ansbach in 1409 and after heavy feuding entered into the service of King Sigismund. In 1410, the death of Rupert, King of the Germans left the throne of the Holy Roman Empire vacant. Sigismund enlisted Frederick's help in obtaining the throne. At the time, Jobst of Moravia ruled Brandenburg and thus was one of the prince-electors who had the right to vote for the new emperor. However, Sigismund disputed Jobst's claim to Brandenburg and his right to vote in the imperial election. Sigismund claimd these rights for himself and designated Frederick to represent him as elector of Brandenburg in the imperial election of 20 September 1410. While Sigismund won this initial vote, Jobst of Moravia won the support of a majority of electors in an election in October 1410 and himself claimed the imperial throne. Jobst's death under suspicious circumstances in January 1411 cleared the way for Sigismund's recovery of Brandenburg and his undisputed election as king of the empire later that year. In gratitude for Frederick's services, King Sigismund made him Oberster Hauptmann and Verwalter der Marken (1411). With an iron hand Frederick fought against the rebellious nobility of the March of Brandenburg (in particular, the Quitzow family) and, in the end, restored security. Frederick also became a member of the Parakeet Society and of the League of Constance.
At the Council of Constance (30 April 1415) Sigismund granted Frederick the titles of Margrave and Prince-elector of Brandenburg. On 21 October 1415 the Brandenburg states meeting in a Landtag asked him to rule in Berlin. The king awarded him the formal enfeoffment of the margravate on 18 April 1417. As Frederick did not agree with the forcible action of Sigismund against the Hussites, relations between them cooled.
Constant feuding with the nobility of Brandenburg led Frederick to withdraw to his castle at Cadolzburg in 1425 and transferred the regency of the margravate to his son John in 1426 (Frederick, however, remained elector). After 1427 he organized the imperial war against the Hussites and helped on the occasion of the Council of Basel substantially in the mediation by the Prager Kompaktaten (30 November 1433).
Upon his death in 1440, Frederick was succeeded as Elector by his second-eldest son, Frederick II.