After the war Oliver Winchester continued to exercise control of the company, renaming it the Winchester Repeating Arms Company, and had the basic design of the Henry rifle completely modified and improved to become the first Winchester rifle, the Model 1866, which fired the same .44 caliber rimfire cartridges as the Henry but had an improved magazine (with the addition of a loading gate on the right side of the receiver, invented by Winchester employee Nelson King) and, for the first time, a wooden forearm. The Henry and the 1866 Winchester shared a unique double firing pin which struck the head of the rimfire cartridge in two places when the weapon was fired, increasing the chances that the fulminate in the hollow rim would ignite the 28 or so grains of black powder inside the case.

Another extremely popular model was rolled out in 1873. The Model 1873 introduced the first Winchester center fire cartridge, the .44-40 WCF (Winchester Central Fire). These rifle families are commonly known as the "Gun That Won the West".

The Model 1873 was followed by the Model 1876 (or "Centennial Model"), a larger version of the '73, which utilized the same toggle-link action and brass cartridge elevator dating from the Henry. It was chambered for longer, more powerful cartridges such as .45-60 WCF, .45-75 WCF, and .50-95 WCF. The action was not strong enough to allow Winchester to achieve their goal of producing a repeating rifle capable of handling the .45-70 Government cartridge; this would not happen until they began manufacture of the Browning-designed Model 1886.

Winchester continued to dominate the American rifle market for decades with the introduction of Models 1876, 1886, 1892, 1894, and 1895 (which featured a box magazine, rather than the tubular magazine found on the previous models). The '76 was a heavier-framed rifle than the '66 or '73, and was the first to be chambered for full-powered centerfire rifle cartridges, as opposed to rimfire cartridges or handgun-sized centerfire rounds. It was introduced to celebrate the American Centennial, and earned a reputation as a durable and powerful hunting rifle. The Canadian Mounties also used the '76 as a standard long arm for many years.

Note: Theodore Roosevelt used an engraved, pistol-gripped half-magazine '76 during his early hunting expeditions in the West and praised it.