Miller was born in Menomonie, Wisconsin, and came to the automotive world through a circuitous path. His early work included a stint at the short-lived Yale Automobile Company and time at Oldsmobile in Lansing, Michigan, where he served as a race mechanic during the early Vanderbilt Cup races. After a disappointing 1906 racing season he relocated to Los Angeles, California, where he opened a small machine shop focused on carburetor manufacture. That business flourished; by the 1910s Miller was earning roughly one million dollars per year from carburetor sales alone.
Miller's inventive instincts went well beyond carburetors. He claimed involvement with an early four-cylinder outboard engine that his neighbor Ole Evinrude subsequently refined into the patented outboard motor. He was also credited with producing the first aluminum pistons and developing aluminum alloys that remained foundational to engine construction for decades, as well as pioneering carburetors and induction systems incorporating Helmholtz resonators.
Miller's carburetor work drew him into the racing world as a repairer and then builder of racing engines. In the early 1920s he constructed his own 3.0-litre four-cylinder engine featuring dual overhead camshafts and four valves per cylinder — a configuration inspired by Duesenberg and Peugeot units he had serviced. Financial backing came from racer Tommy Milton, but it was Jimmy Murphy who first demonstrated its potential, powering a Duesenberg to victory at the 1922 Indianapolis 500.
From that foundation Miller progressed to building complete single-seater race cars using supercharged versions of his 2.0-litre and 1.5-litre (122 and 91 cubic inch) engines. Between 1923 and 1929 these cars and engines dominated the Brickyard, scoring wins in 1926 and 1928 in outright Miller chassis. Miller engines continued winning at Indianapolis through 1938, accumulating seven further victories including two more in Miller-built cars in 1930 and 1932.
Outside oval racing, Miller engines powered speedboats to multiple race wins and world water speed records. Legendary hydroplane racer Gar Wood was among those who raced successfully with Miller power on the water.
Despite his technical genius, Miller struggled financially. He declared bankruptcy in 1933. His shop foreman and chief machinist, Fred Offenhauser, purchased the business and continued developing the engine lineage under the Offenhauser name; those engines went on to dominate American oval racing through the 1980s.
After bankruptcy, Miller partnered with Indianapolis 500 enthusiast Preston Tucker. In 1935 they formed Miller and Tucker, Inc., whose first major commission was to build ten modified Ford V-8 racers for Henry Ford. Insufficient development time left all ten cars sidelined after their steering boxes — mounted too close to the exhaust — overheated and locked up at the Speedway. Privateers later solved the problem and examples raced at Indianapolis as late as 1948.
Miller and Tucker subsequently moved to Indianapolis, where the partnership extended into military vehicle design. Their Tucker Combat Car, capable of 115 mph on pavement and 65 mph on rough terrain, featured a power-operated gun turret that the United States government purchased and deployed in applications ranging from the Boeing B-17 and B-29 to PT boats and landing craft. Miller also drew on Combat Car suspension elements when contributing to the development of the first Jeep at American Bantam.
Harry Miller died on May 3, 1943, at Grace Hospital in Detroit, aged 67. Tucker helped Miller's widow meet the funeral costs.
Griffith Borgeson, the leading chronicler of American racing history, called Miller "the greatest creative figure in the history of the American racing car." The engine lineage he started — developed by Offenhauser and later turbocharged — remained competitive at Indianapolis for more than fifty years after Miller's death, a record of longevity unmatched by any other American racing engine family.
Miller was inducted into the National Sprint Car Hall of Fame in 1990, the Motorsports Hall of Fame of America in 1999, and the Automotive Hall of Fame in 2003. He was honored posthumously at the 1993 Monterey Historic Automobile Races.