Virginia had little impact on the Royal Navy's designs. By the time she had been commissioned, the RN had constructed several ironclads, starting with the Warrior, which outclassed her near completely. Compared to Warrior, Virginia was slower, less well armed and armoured, and less seaworthy. With no masts and little freeboard, Virginia was incapable of crossing oceans, while Warrior could easily deploy to wherever the Royal Navy needed. By the end of 1862, the RN would have constructed or converted 9 ironclads, all on a similar scale to Warrior. Just four years later, that number had doubled.

Monitor, though, was more influential. Monitor and her successors were impressive ships, with considerable resistance to enemy fire and an ability to deal heavy damage to a target. However, it was unsuitable for the RN's requirements. Monitor had a lack of ventilation belowdecks and was a poor seaboat. It could not cross oceans or travel far from land, both things the RN would need given its worldwide commitments. As such, the RN built no ships to the classic 'Monitor' design. Instead, the RN's chief designer, Edward Reed, solved the flaws of the 'Monitor' design by adding an armoured breastwork amidships, with turrets, ventilators and other openings positioned on it, with the first such ship being the Cerberus of 1867. This created a monitor capable of operating at sea, limited only by coal supplies. The RN's battleships of the late 19th Century would follow in Cerberus's footsteps. The breastwork would be extended to the edge of the hull, and then forward to its ends. The turrets would be replaced with lighter barbettes (rotating gun platforms with a ring of armour surrounding them), allowing for the freeboard to be raised. When the barbettes were given an armoured covering or gunhouse, the classic 'Pre-Dreadnought' was formed.

The battle between Monitor and Virginia did have other influences, though. Hampton Roads showed the difficulty of sinking ironclads with traditional weapons, as the two ships spent the battle fruitlessly bombarding each other to little avail. To this end, the RN spent a considerable amount of time trying to improve the capabilities of its guns. A major step forward came in 1863, when General Sir William Palliser invented the chilled iron shot, which was soon named after him. This was an elongated, somewhat conical, projectile made of cast iron, cast in a chilled mould to harden the outside. They were good against wrought iron armour, but tended to break up when fired at steel. They could contain a black powder bursting charge. However, this often exploded when piercing armour, so was left out when expecting to face an armoured target. From 1863-1865, Woolwich Arsenal developed a series of rifled muzzle loaders (RML). These guns had six to nine rifling grooves, which would engage with bronze studs on the projectile. Firing Palliser shot, they could penetrate up to their calibre in wrought-iron armour at 1000 yards. They were effective but cheap guns, though the rifling system caused considerable erosion of the bore. Hampton Roads also suggested the value of ramming; Virginia's ramming of Cumberland caused the latter to sink more quickly than any gun engagement could. A number of steam rams also operated with some success during the riverine campaigns of the Civil War. These successes were reinforced by Battle of Lissa in the Austro-Prussian War. In this battle, eight ramming attempts culminated in the sinking of the Italian Re d'Italia by the Austrian Erzherzog Ferdinand Max. Combined, this enshrined ramming as a key tactical option for much of the late 19th Century - even the Canopus class of 1896-8 were given rams.

The most important naval lesson for the RN from the American Civil War, though, did not involve ironclads. Instead, it focused on commerce raiding and cruiser warfare, which used mainly unarmoured ships. The Royal Navy, in the years running up to the Civil War, had neglected to build cruisers (here meaning the general category that includes frigates, sloops and corvettes), favouring ironclads like Warrior. Similarly, commerce raiding and trade protection had been neglected in RN tactical thought. However, during the war, both the Union and Confederate navies carried out significant cruiser warfare campaigns. The USN carried a significant, and ultimately successful, blockade of the Confederate coast, capturing 1149 blockade runners and sinking another 335. The Confederates, meanwhile, used privateers and cruisers to harass Union trade. The Confederate cruisers captured or sank 209 ships, while their privateers captured another 52. While this was small compared to the number of ships in the Union merchant marine, it had an outsize effect on it, as ships were laid up, or transferred to other flags - just under half a million tons of Union shipping was transferred to the British flag (this represented about a fifth of the Union's sea-going merchant fleet in 1860). Several key lessons could be learned from these campaigns. The Union campaign showed the need for large amounts of cruisers to maintain an effective blockade. The Confederate campaign showed that raiders could operate world-wide, that raiders could not be effectively starved of coal (as they could take it from prizes or buy from neutrals), and that neutral nations might not be willing to properly enforce the rules of neutrality. The campaign also showed the difficulty of finding and capturing raiders, with the USN finding it difficult to locate their Confederate prey.

The RN's response to these successes was to start construction on a number of new classes of cruiser. They attributed Confederate success to a lack of fast Union cruisers. The Amazon, Blanche and Druid classes of corvette were built to outrun the fastest raiders available. In 1866, the USN commissioned the Wampanoag class of fast frigates. They had been ordered in 1863 "to sweep the ocean and chase and hunt down the vessels of an enemy", a description that could apply equally to British merchants as it did to Confederate cruisers. Theoretically capable of 16 knots and well armed (though in fact, they could not sustain the speed for long and could not mount a chase gun, a necessity for commerce raiding), they were a significant threat. In return, the RN built three frigates of the Inconstant class. These were generally excellent ships for their designed role, fast, seaworthy and long-ranged, while carrying a heavy enough armament to deal with any raider. The Inconstants were the brainchild of Vice Admiral Robert Spencer Robinson, Controller of the Royal Navy, who was responsible for drawing up the RN's trade protection doctrine. To him, there were two main threats to trade; warships, which could clear British cruisers from the sea, and privateers, which could snap up the resulting unprotected trade. The necessary response, as expounded by Robinson to the 1871 Committee on Design, was for corvettes and sloops to protect trade against privateers and smaller warships, while the frigates drove off any warship. In this statement, Robinson seems at times to be advocating for the establishment of a convoy system, but later argued that such a system would be impractical for steam merchants. This system would provide the blueprints for the RN's response to commerce warfare into the 20th Century.