The Chamber of Whitestone is a ruling body of Whitestone. Lord Percival de Rolo established the council after He and Vox Machina defeated the Briarwoods. The Council currently consists of seven members, including four chosen from community leaders and three nobles.
- The Guardian of Woven Stone: The leading figure on the council, responsible for higher civil justice, community unification and internal government. Percival de Rolo's intentions were for this position to always be held by a member of the De Rolo family.
- The Steward of Sunblessed Gifts: Responsible for local farming, goods and distribution.
- The Curator of Fortune’s Bounty: Responsible for all major commerce including local trade and trade with foreign entities.
- The Keeper of Divine Virtue: Responsible for religious organizations.
- The Pale Lord of Wardship: Responsible for law enforcement matters and commands the Paleguard. They also act as judge on smaller matters of civil justice, and are responsible for defending the city during times of war.
- The Sophist of Native Ingenuity: Responsible for infrastructure of the city and castle.
- The Grand Mistress of the Grey Hunt: Responsible for diplomatic relations, and rooting out dangers within the Parchwood. This title has historically been tied to the Lord/ Lady of the Third House of Whitestone, a title which was given to Vex'ahlia by Percy well before their marriage. 
- Cassandra de Rolo acts as The Guardian of Woven Stone.
- Percival de Rolo acts as The Sophist of Native Ingenuity.
- Lady Vex'ahlia acts as The Grand Mistress of the Grey Hunt.
- Critical Role: Tal'Dorei Campaign Setting, p. 32-33.