Over the past three decades, Richard A. Epstein has repeatedly argued—with analytical rigor and astonishing erudition—that governments govern best when they limit their actions to protecting liberty and property. He is perhaps best known for “Takings,” his 1995 book on the losses that regulations impose on property owners. Of late, he has exposed the flaws of a government-administered health system.

In “The Classical Liberal Constitution,” Mr. Epstein takes up the political logic of our fundamental law. The Constitution, he says, reflects above all John Locke’s insistence on protecting natural rights—rights that we possess simply by virtue of our humanity. Their protection takes concrete form in the Constitution by restricting the federal government to specific, freedom-advancing and property-protecting tasks, such as establishing a procedurally fair justice system, minting money as a stable repository of value, preserving a national trade zone among the states, and, not least, guarding the rights listed in the Bill of Rights.

Mr. Epstein believes that constitutional law lost its way when it began to embrace a Progressive vision, according to which rights are created by a supposedly benevolent state. Starting especially with the New Deal legislation of the 1930s, the federal government has passed laws that redistribute wealth, water-down procedural protections for property, and dictate the relations between employers and employees. The premise of such laws is that government should establish a pattern of social justice. By such logic, the government may declare rights that are in no way natural (like the right to an old-age pension) and remove others that are fundamental (like freedom of association).

The antidote, for Mr. Epstein, is a reassertion of liberal principle aimed at helping individuals realize joint prosperity through trade and contract. In “The Classical Liberal Constitution,” he interprets provisions that are often murky in their application, like the First Amendment’s prohibition of laws “respecting an Establishment of religion.” Here he rejects a strict separation of church and state to make room for religion in the public sphere, on the grounds that accommodating many faiths provides mutual gains—a hallmark of classical liberalism.

The Classical Liberal Constitution

By Richard A. Epstein
(Harvard, 684 pages, $49.95)

He also uses liberal principle to judge which Supreme Court precedents should be retained and which discarded. He would keep the precedents that vindicate liberty, like protecting a right to contraception, even if this particular right cannot be rooted in the Constitution’s text. Similarly, he acknowledges that the Constitution did not foresee judicial supremacy—the courts’ power to bind the other branches of government by its precedents. But he applauds judicial supremacy because, in his view, it generally restrains the overweening state.

In its ambition and range, “The Classical Liberal Constitution” is comparable with John Hart Ely’s magisterial “Democracy and Distrust” (1980). Just as Ely claimed that representative government is the objective that unlocks the meaning of the Constitution’s disparate clauses and amendments, Mr. Epstein claims to discover the interpretive key in classical liberalism—in the call for a limited government protecting natural rights.

To be sure, the Framers were very much aware of Locke, and liberalism is central to the Constitution’s meaning. But Mr. Epstein never shows that Locke’s liberalism tracks his own or that it was the dominant influence on the Framers. Other influences included Montesquieu, who stressed a balance of powers, and some of the Framers adhered to the civic-republican tradition, whereby one role of government was to cultivate virtue. What is more, the Constitution reflects the lived experience of Americans and their forebears. The Bill of Rights derives in part from quarrels among English religious sects and the abuses of the Star Chamber. The very wording of the Bill of Rights often expresses this long history.

A case in point is the Second Amendment, which declares: “A well regulated Militia, being necessary to the security of a free State, the right of the people to keep and bear Arms shall not be infringed.” The Supreme Court recently declared that the amendment protects the right of citizens in the District of Columbia to possess a handgun in their home. Mr. Epstein rejects this decision on the grounds that the District is not a “state.” But the amendment’s preamble, in which the phrase “a free State” appears, announces a political proposition. It thus likely refers to political entities in general, not specific jurisdictions, and Mr. Epstein provides no historical or scholarly support for his novel suggestion.

Mr. Epstein is at its strongest when he combines his analytical powers with the historical research of others, as he does when he discusses the clause that gives Congress the authority to make all laws “necessary and proper” to executing the powers enumerated in the Constitution. This clause has been used over and over again to expand the authority of the federal government. Mr. Epstein provides evidence that the Framers would not have considered legislation “proper” if it exercised an unenumerated power of substantial scope. It is one thing for the government to criminalize stealing the mail as part of its authority to establish post offices. It is quite another for it to penalize citizens for not participating in a market, as it did when it required individuals to buy insurance as part of its regulation of commerce under the Affordable Care Act. Mr. Epstein’s argument here is based on historical understanding as well as principle.

The Constitution, as Mr. Epstein argues, provides us with rights to individual liberty and property, but it also gives us the right of collective self-government. While there will never be an easy synthesis of both inheritances, he vividly shows us how constitutional law would look if we gave priority to individual rights—something that we have not done for almost a century.

Mr. McGinnis is a professor of law at Northwestern University.