Wakefield Tower, built between 1220 and 1240, by Henry III provided royal accommodations for Henry and his son Edward I. The Tower later became a document depository and, for a time, housed the Crown Jewels.

St. Thomas' Tower, built by Edward I between 1275 and 1279, provided accommodations for the King and a new water entrance to the Tower. Under St. Thomas' Tower is the river entrance, now called Traitor's Gate because it was through here that prisoners, such as Anne Boleyn, Sir Thomas More and Princess Elizabeth (later Queen Elizabeth I), accused of treason, arrived.

Before the building of St. Thomas' Tower and the outer walls along the river, the Bloody Tower (originally called the Garden Tower) stood by the edge of the river and controlled the entrance to the castle. After 1280, with the construction of the Outer Ward and the new Wtergate, the Bloody Tower became the principal access to the Inner Ward. Under the 19th century arched bridge that joins St. Thomas' Tower with Wakefield Tower are the remains of Henry III's earlier private Watergate.

The Bloody Tower, built in the early 1220's with an upper level constructed in about 1360, housed prisoners, such as Thomas Cranmer and William Laud, both Archbishops of Canterbury, Lord Chancellor, Judge Jeffreys and Sir Walter Raleigh. The Bloody Tower is where the sons of King Edward IV, Edward (12 years) and his brother Richard (10) were held under the protection of their Uncle Richard, Duke of Gloucester. The princes were lodged in the tower after their father's death in 1483. During the preparations for Edward's coronation, the two princes disappeared. Their Uncle was subsequently crowned Richard III. Much has been made about the Princes' fare and Richard's involvement in their deaths but no conclusive evidence has ever been produced.