Several supported Union forces along the Mississippi River in mid-1864 before participating in the Battle of Mobile Bay in August.

Chickasaw and Winnebago bombarded Confederate coastal fortifications during the battle and during subsequent operations as well as engaging the ironclad Tennessee II.

The Milwaukee-class monitors had their origin in an order from Gideon Welles, Secretary of the Navy, to Commodore Joseph Smith, Chief of the Bureau of Yards and Docks, on 16 April 1863 to recommend four more river ironclads that could mount four 11-inch (279 mm) Dahlgren guns on a draft no more than 6 feet (1.8 m).

[5] The ships' main armament consisted of four smoothbore, muzzle-loading 11-inch Dahlgren guns mounted in two twin-gun turrets.

Below the deck the side of the Eads turret was only a single layer thick and had holes through which the guns were loaded.

The sides of the hull consisted of three layers of one-inch plates, backed by 15 inches (380 mm) of pine.

The deck was heavily cambered to allow headroom for the crew on such a shallow draft, and it consisted of iron plates .75 inches (19 mm) thick.

[7] Chickasaw and Winnebago, the first two ships to be commissioned, spent some time patrolling the Mississippi River and supporting Union forces operating along its length before they were transferred to the West Gulf Blockading Squadron in early July 1864 to support the impending attack on the defenses of Mobile, Alabama[9][12] Rear Admiral David Farragut organized the four monitors present into a separate column leading his wooden ships to engage Fort Morgan while the other ships proceeded into the Bay itself.

[13] Tecumseh struck a torpedo in front of the fort and a small boat from the gunboat Metacomet rescued 10 survivors and delivered them to Winnebago.

[14] The latter's aft turret had jammed during her bombardment of Fort Morgan while Chickasaw's funnel had been riddled with holes, significantly reducing her speed.

The monitors were not initially engaged, but Chickasaw managed to assume a position by the Tennessee's stern and fired repeatedly at point-blank range.