- "It is difficult for historians to declare a certain date for the foundation of Wayrest. A settlement of some variety had been in existence where the Bjoulsae River feeds the Iliac Bay possibly since the 800th year of the First Era." — Sathryr Longleat, "Wayrest, Jewel of the Bay"
The city is split into seven districts. In the northern part of the city, running from the north gate to the east gate, lies the Residential District where many of the homes are situated. The city stables and an inn can be found by the north gate. West of the river and south of the Residential District lie the Merchant District and Market Square, which contain many of the city's traders and merchants, as well as the Fighters Guild. In the west, the Temple of the Divines and Wayrest Castle dominate the Temple and Palace Districts respectively, while in the east, the Wayrest Treasury building marks the Banking District. The west gate, leading towards Farangel's Landing and the At-Tura Estate, can be found in the Palace District, just past Wayrest Wayshrine. Just inside the south gate, the Mages District houses the Mages Guild and the Chironasium. Outside the south gate, on the banks of Iliac Bay, sit Wayrest Docks, from which it is possible to buy passage to Alik'r.
- Another Omen: Warn High King Emeric of the emergent threat in Gavaudon.
- The Dangerous Past: Search a Dwemer ruin for signs of an ancient weapon.
- The Debt Collector's Debts: Help a debt collector settle his debt with his boss.
- A Gang of Thugs: Help the captain of the Wayrest Guard rid the city of a gang of bullies.
- The Missing Prophecy: Rescue the Oracles of Azura from their Daedric prisons.
- One Last Game: Solve a riddle to find an inheritance.
- Pursuing the Shard: Head to Wayrest to inform High King Emeric of the theft from the Abbey.
- The Road to Rivenspire: Head to Rivenspire on the order of High King Emeric and assess the situation between the noble houses.
- Simply Misplaced: Recover two items that the Mad God claims to have misplaced.
- Taking the Undaunted Pledge: Visit the Undaunted Enclave and sign the Tome of the Undaunted.
- Vaermina's Gambit: Face the Night Terror and end the threat to Stormhaven.
Shops and Services
- The Bough and Birdsmouth — A carpentry store in Wayrest Residential District.
- Chironasium — An alchemy and enchanting store in the Wayrest Mages District.
- Chironasium Chromatics — An outfit station in Wayrest.
- Cloudy Dregs Inn — A tavern in Wayrest Residential District, near the north gate.
- Fighters Guild Hall — A guildhall located near Wayrest Market Square.
- Foal's Rest Stables — A stable by Wayrest's north gate.
- The High King's Forge — A smithy in Wayrest Residential District.
- Lion's Crown Outfitters — A store north of Wayrest Market Square.
- Mages Guild Hall — A guildhall located in Wayrest Mages District housing the local branch of the Mages Guild.
- Merchant District — A marketplace west of the river in Wayrest.
- North Gate Novelties — A general goods trade stall located by Wayrest north gate.
- Red Squall Armory — A store located by Wayrest Market Square.
- Rededication Shrine — A rededication shrine in Wayrest.
- Stormhaven's Trade Coster — A collection of guild kiosks located near the west gate of Wayrest.
- Wayrest Outlaws Refuge — An outlaws refuge hidden beneath Wayrest.
- Wayrest Treasury — A bank in Wayrest Banking District.
- Transport Services
- Caravan: Star-Gazer Herald (Belkarth)
- Covenant Navigator: Azoufah (Rivenspire, Glenumbra, Grahtwood, Deshaan)
- Dock: Zihlijdel (Alik'r Desert)
- Harbor Skiff: (Abah's Landing)
- Wayrest Sewers — A group dungeon found under the city of Wayrest in Stormhaven
- Wayrest Wayshrine — Located in central Wayrest.