From his maternal grandfather, he inherited still a child the title of 3rd Count of Arraiolos, and later, by royal decree dated from May 25, 1455, King Afonso V of Portugal granted him the new title of 1st Marquis of Vila Viçosa.

In 1432, the young Ferdinand of Arrailos was called upon by King John I for consultation on a project, promoted by Prince Henry the Navigator, to launch a campaign of conquest against the Marinid sultante of Morocco. Ferdinand submitted opinion was almost wholly against the project. When the project was picked up again during the reign of King Edward in 1436, Ferdinand once again reiterated his objections. Nonetheless, despite his opposition, Edward appointed Ferdinand as constable of the nobles for the 1437 expedition to seize Tangier. Although the expedition was under the overall command of Henry the Navigator, Edward felt Ferdinand's military expertise was necessary to make up for Henry's inexperience. The Tangier campaign was a debacle. After failing to conquer the city by assault, the Portuguese expeditionary army was surrounded and starved into submission by a Moroccan relief army. In return for being allowed to withdraw his troops unmolested, Henry agreed to a treaty to deliver Ceuta back to the Marinids. For the fulfillment of the treaty, Henry handed over his own brother, the royal infante Ferdinand the Saint Prince as a hostage to the Moroccans.

Back in Portugal, Ferdinand of Arraiolos led the opposition to the treaty. At the Cortes of Leiria assembled in early 1438 by King Edward, Ferdinand of Arraiolos rallied the nobles and took the floor, urging them to refuse to surrender Ceuta. Ferdinand claimed the treaty was signed under duress and invalid. It was largely because of Ferdinand's energetic campaign that the Cortes rejected ratification and told the king to find some other way of securing Prince Ferdinand's release (none was found - Ferdinand the Saint Prince would die in Moroccan captivity in 1443).

Ferdinand of Arraiolos was nominated Governor of Ceuta from 1445 until 1450.

In 1458, he took part, along with his sons, in the expedition that conquered the Moroccan city of Alcácer Ceguer.

In 1460, as his older brother Afonso, died without legitimous issue, he became the 5th Count of Ourém and the House of Braganza heir and, one year later, following his father’s death (1461), he also became the 2nd Duke of Braganza, 9th Count of Barcelos and 3rd Count of Neiva and 3rd Lord of Faria.

In 1471, when King Afonso V fled again to North Africa to conquer the city of Arzila, he remained in mainland Portugal as regent of the Kingdom.

Fernando I of Braganza married, on 28 December 1429, Dona Joana de Castro (c. 1410 – Lisbon, 14 February 1479) (daughter and heir of Dom João de Castro, 2nd Lord of Cadaval), and they had nine children.