By 1925, his development aircraft had become reliable, and he began to demonstrate it in France, England, and the United States. On October 20, 1925, his pilot Frank T. Courtney flew the autogyro at Britain's Royal Aircraft Establishment near Farnborough during tests for the British Air Ministry.

Later that year, Cierva formed the Cierva Autogiro Company, Ltd., in Great Britain. Courtney toured Europe, and early in 1926, he demonstrated the gyro for the French at Villacoublay Airdrome with at least one crash. In September 1926, he flew at Tempelhof near Berlin. On September 18, 1928, Cierva flew an improved autogyro 25 miles (40 kilometers) across the English Channel from Croydon to Le Bourget Airfield near Paris in 18 minutes at 4,000 feet (1,219 meters). He then took a leisurely trip 3,000 miles (4,828 kilometers) across Europe that drew crowds everywhere.

A crash in February 1927, led to an improvement in rotor hub design. A "drag hinge" was incorporated at the hub to allow each blade to drag back a little or pivot forward slightly as it rotated. This relieved the stresses and was another step in developing the fully articulated hub used on many modern helicopters. Another innovation was the development of a mechanical starter to bring the rotor up to the necessary speed for takeoff.

During the next decade, some 500 gyros were built around the world. In Britain, the A.V. Roe, de Havilland, Weir, and Westland companies produced them. In Germany, Focke-Wulf built the crafts; in France, it was the Loire Company, and in Russia, The Central Aerohydrodynamic Institute (TsAGI). In 1928, Harold Pitcairn, who had been involved with aviation in the United States since 1914, negotiated successfully with Cierva, purchased a Cierva model C-8 autogyro, and brought it to the United States for test and evaluation. It flew at Bryn Athyn (Pitcairn Field), Willow Grove, Pennsylvania, on December 19, 1928.

In February 1929, Pitcairn purchased the U.S. rights to Cierva's inventions and the autogyro patents then existing and established the Pitcairn-Cierva Autogiro Company for licensing its manufacture in the United States. Kellett, another U.S. aviation company, also manufactured gyros in the United States.

In August 1929, the first public demonstration of a Cierva machine took place in the United States at the Cleveland Air Races. The two-person open cockpit aircraft cruised at 75 miles per hour (120 kilometres per hour) and had a top speed of 90 miles per hour (145 kilometres per hour). In 1930, an autogyro led an "air parade" during an airshow at Newark Airport in New Jersey. Later, a special demonstration was given for Thomas Alva Edison, who was enthusiastic about the device.

The autogyro had a few years of popularity in the United States. On February 12, 1931, the Detroit News placed the first order for a commercial autogyro in the United States, the Pitcairn PC A-2. On April 8, 1931, Amelia Earhart set a world's altitude record for autogyros, climbing to 18,415 feet (5,615 meters). And on April 22, the autogyro received more publicity when veteran Pitcairn pilot Jim Ray landed on the White House lawn and took off again for the ceremony at which President Herbert Hoover presented the Collier Trophy to manufacturer Harold Pitcairn "for the greatest achievement in aviation, the value of which has been demonstrated by actual use in the preceding year." Pitcairn built 51 autogyros in 1931 and developed a number of models for the U.S. Navy as well as some models intended for private owners.

The development of the "direct control" rotor on a modified Cierva C-19 in 1932 led to the elimination of ailerons and stub wings. With this system, the rotor was mounted so that it could be tilted, resulting in a force that would pull the gyro in that direction. This was a great advance over the existing airplane-type control surfaces.

The next major improvement occurred in 1934. A Cierva autogyro was developed with a device to produce a vertical "jump" takeoff. This brought the gyro's design much closer to the design of the true helicopter. The new device was successful, and for the first time, a rotating-wing flying machine existed that could actually lift itself vertically into the air.

In 1935, Austrian experimenter Raoul Hafner created the AR III Hafner Gyroplane, first flown in Britain. This vehicle had hinged rotors and featured both cyclic control and collective control, in which the pitch of all rotors was changed simultaneously to increase or decrease lift. The Hafner gyro could rise and continue to climb at a fairly steep angle.

The development of cyclic pitch control was a major improvement. Instead of "rocking" the rotor head, this approach called for feathering—increasing or decreasing the pitch of the blades in cycles as they turned. Each blade would assume a high pitch position on the advancing side of the rotor's circle and a low pitch on the retreating side. This meant an increase in lift on one side and a decrease in lift on the other side. Feathering eliminated the need for hinges so that the blades could move up and down and allowed for a rigid rotor.

Cierva and Pitcairn licensed the Kellett Autogyro Corporation of Philadelphia to build autogyros for the U.S. Army. Kellett developed the YG-1 in 1935, which became the Army's first rotary-winged aircraft. Although autogyros saw little service with the U.S. military. Cierva autogyros did see some limited service in the armed forces of France, the Soviet Union, and Japan for forward observation and artillery spotting during World War II. They also played a small but important role in Britain where they were useful in calibrating the vital air-defence radar network.

The autogyro saw some use for airmail. On July 6, 1939, Eastern Air Lines began the world's first scheduled air mail service by a rotary winged aircraft, using a Kellet gyro to fly from the roof of the Philadelphia Post Office to the airport at Camden, New Jersey. This experimental service lasted about one year.

While still used to some extent, autogyros have been plagued by one major problem that contributed to their limited acceptance. The phenomenon called ground resonance develops when the rotor blades move out of phase with each other and cause the rotor disc to become unbalanced. If not corrected, serious damage can take place in only a few seconds. Ground resonance can occur only when the gyro is on the ground and happens when a shock, such as from a hard landing, is transmitted to the rotor system. If the centre of gravity moves from the centre of rotation, the entire vehicle can become unbalanced.