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Dillon was born in Northampton, Montgomery County, New York (now part of Fulton County, New York). He studied medicine at Iowa State University at the age of 19. Shortly after beginning his practice, he abandoned it to read law, and was admitted to the Iowa bar in 1852. He was elected as the Scott County prosecutor after a brief private practice in 1853, and was then elected to a judgeship in Iowa's 7th Judicial Circuit in 1858. He was elevated to the Iowa Supreme Court in 1862 and served until 1869, when he was appointed by President Grant to the United States Circuit Court which became the Eighth Circuit.

While on the federal bench, Dillon wrote Municipal Corporations (1872), which was one of the earliest treatises to systematically study the subject, and which remains highly influential to the present. He was also the author of Removal of Cases from State Courts to Federal Courts and Municipal Bonds, both in 1876. On February 17, 1876, Justice Dillon ruled Ulysses S. Grant's deposition for Orville E. Babcock was admissible in court during the Whiskey Ring graft prosecutions. After leaving the Circuit Court, Dillon was a professor at Columbia Law School from 1879 until 1882, where he taught real estate and equity. He then taught at Yale Law School from 1891 until 1892, during which time he also served as the president of the American Bar Association. Dillon then returned to private practice until his death in 1914 in New York City.

A memorial fountain to Dillon was erected in downtown Davenport, Iowa in 1918, carved of Indiana limestone in Romanesque style, by sculptor Harry Liva.

Dillon's oldest son, Hiram Price Dillon (1855 – 1918), also became a lawyer in Iowa, and a Master of Chancery in federal court. John F. Dillon had a sister who married John B. Jordan, a Davenport, IA merchant. That marriage produced a daughter Jennie, who married Louis Stengel from across the river in Rock Island, IL. Louis and Jennie Stengel moved to Kansas City, and had a son, Charles Dillon Stengel, who was named after the Judge. Casey went on to quite a career in baseball, first as a player, and then as a manager of the New York Yankees.

The theory of state preeminence over local governments was expressed as Dillon’s Rule in an 1868 case: "Municipal corporations owe their origin to, and derive their powers and rights wholly from, the legislature. It breathes into them the breath of life, without which they cannot exist. As it creates, so may it destroy. If it may destroy, it may abridge and control. Clinton v Cedar Rapids and the Missouri River Railroad,(24 Iowa 455; 1868). As opposed to Dillon's Rule, the Cooley Doctrine expressed the theory of an inherent right to local self determination. In a concurring opinion, Michigan Supreme Court Judge Thomas M. Cooley in 1871 stated: “[L]ocal government is a matter of absolute right; and the state cannot take it away.” People v. Hurlbut, (24 Mich 44, 95; 1871).

In Municipal Corporations (1872), Dillon explained that in contrast to the powers of states, which are unlimited but for express restrictions under the state or federal constitution, municipalities only have the powers that are expressly granted to them. This formulation of the scope of municipal power came to be known as the "Dillon Rule," which states that municipal governments only have the powers that are expressly granted to them by the state legislature, those that are necessarily implied from that grant of power, and those that are essential and indispensable to the municipality's existence and functioning. Any ambiguities in the legislative grant of power should be resolved against the municipality so that its powers are narrowly construed. However, when the state has not specifically directed the method by which the municipality may implement its granted power, the municipality has the discretion to choose the method so long as its choice is reasonable.

Hundreds of U.S. court decisions to the present day have employed the Dillon Rule to determine the scope of municipal powers and rights. Critics of the Rule have argued that it imposes unreasonable constraints on the ability of communities to govern themselves and so undermines democracy, and even that local self-government is a matter of natural right that does not need to be conferred by higher political structures. It has also been suggested that Dillon's approach derived from the contemporary view that cities were inherently corrupt political organs. This was perhaps an often well-deserved judgment during his time, especially considering the extensive business ties and even investments of numerous cities and their leaders in the late 19th century. Deviations from the Dillon Rule remain in the minority, however, despite the significant decrease in the public perception of municipal corruption.

The Supreme Court of the United States cited Municipal Corporations and fully adopted Dillon's emphasis on state power over municipalities in Merrill v. Monticello, 138 U.S. 673 (1891), reaff'd. Hunter v. Pittsburgh, 207 U.S. 161 (1907), which upheld the power of Pennsylvania to consolidate two cities against the wishes of the majority of the residents in one. The Court's ruling that states could alter or abolish at will the charters of municipal corporations without infringing upon contract rights heavily relied upon Dillon's separation of public, municipal corporations from private ones.

Pittsburgh Regionalist David Y. Miller argues that Dillon hit upon a central paradox defining American cities: having great political authority while having little legal legitimacy. He quotes Dillon as calling municipalities "mere tenants at will of their respective state legislatures" which could be "eliminated by the legislature with a stroke of the pen." And yet, Dillon also said that eliminating local government would be "so great a folly, and so great a wrong."