He earned a B.A. in History and Government from Cornell University, an M.A. in International Relations from Yale University, and a Ph.D. in U.S. History from Stanford University.

Alterman began his journalism career in 1983, freelancing originally for The Nation, The Washington Monthly, The New Republic, Harper's, Le Monde diplomatique, and later, Vanity Fair, The New York Times Magazine, and The Atlantic Monthly, among others, while working as a senior fellow for the World Policy Institute in New York City and Washington, DC. He published his first book, Sound & Fury: The Making of the Punditocracy, which won the 1992 George Orwell Award, while studying for his doctorate in US history in Stanford in 1992. Shortly after that he became the Washington Correspondent for Mother Jones, and soon thereafter Rolling Stone, before returning to The Nation as a columnist in 1995. Alterman has also been a contributing editor to ELLE, and a regular columnist for Worth and the London Sunday Express.

Alterman was hired by MSNBC in 1996, both appearing as a commentator on the cable channel and writing a column posted on its website. In 2002 MSNBC engaged him to create the blog daily Altercation, one of the first blogs hosted by a mainstream media news organization. In September 2006, after a ten-year association, Alterman and MSNBC parted ways. Media Matters for America hired him as a Senior Fellow and agreed to host Altercation, effective September 18, 2006. Regular contributors to his blog Altercation include sportswriter Charlie Pierce and historian and military officer Robert Bateman. On December 22, 2008 Alterman announced that Altercation would be moving to The Nation's website in 2009, and would appear on a less regular basis than its previous Monday through Friday schedule.

During this period Alterman also published a number of books, including the national best-sellers What Liberal Media? The Truth About Bias and the News (2003, 2004), and The Book on Bush: How George W. (Mis)leads America (2004). The others include: Who Speaks for America? Why Democracy Matters in Foreign Policy, (1998), and a second edition of Sound & Fury (2000). His It Ain't No Sin to be Glad You're Alive: The Promise of Bruce Springsteen (1999, 2001), won the 1999 Stephen Crane Literary Award. In September 2004, Viking Press published A History of Official Deception and its Consequences —- a version of his doctoral dissertation —— on lies of major consequence told by Presidents Franklin D. Roosevelt, John F. Kennedy, Lyndon Johnson, Ronald Reagan, and George W. Bush.

Alterman has taught journalism at both New York University and Columbia University. Since the fall of 2004, he has been a Professor of English at Brooklyn College, where he teaches courses in media and media history. In 2007 he was named a CUNY Distinguished Professor of English at Brooklyn College and Professor of Journalism at the CUNY Graduate School of Journalism. He is also a Senior Fellow at the Center for American Progress, Media Matters for America, and remains one at the World Policy Institute in New York.

Alterman's academic expertise is American history. He has said "I have an historical context for understanding what is going on. I can see that a lot of things that are happening have happened already. The New York Times and Newsweek write stories as if there's no history. What are we but our histories?" He also works as a history consultant to HBO Films.

His seventh book, published in 2008 by Viking was called Why We're Liberals: A Political Handbook for Post-Bush America. Also in 2008, Alterman also published a lengthy essay in the New Yorker on the decline of American newspapers and the future role of new media news sites.

He is perhaps best known for his media criticism, which is the subject of two of his books. He writes a political column for The Nation and a weekly column for the Center for American Progress website. In contrast to conservative media commentators, Alterman argues that the press is biased against liberals rather than biased in their favor. He was called "the most honest and incisive media critic writing today" in the National Catholic Reporter, and the author of "the smartest and funniest political journal out there," in The San Francisco Chronicle. In 2008, Alterman also became a regular columnist to the Jewish magazine Moment, where he writes regularly about Jewish issues. In 2009, he also became a regular contributor to The Daily Beast. He appears in the award-winning documentary on Lee Atwater, The Lee Atwater Story. In the film, Eric says "Race is poison, but it is poison that works for their side. People vote their fears and not their hopes, and Lee understood that."

He is also an occasional contributor to BloggingHeads.tv, where he often takes part in video discussions with other media personalities.

Alterman identifies himself as the most right-leaning out of the people at The Nation, and he says that he frequently gets pressure from both sides about specific issues. His critics have called him a member of the Israel lobby.

Alterman was and remains a critic of Ralph Nader for Nader's actions in the 2000 U.S. Presidential Election, arguing that Nader is to blame for the election of George W. Bush because of vote splitting. He has called Nader "Bush's Useful Idiot," myopic, and a deluded megalomaniac. In the documentary An Unreasonable Man, he is quoted as saying:

The man needs to go away. I think he needs to live in a different country. He’s done enough damage to this one. Let him damage somebody else's now.