"I wish to reaffirm the great value of academic freedom," Benedict told hundreds of educators gathered at Catholic University of America.
"Yet it is also the case that any appeal to the principle of academic freedom in order to justify positions that contradict the faith and the teaching of the church would obstruct or even betray the university's identity and mission," he said.
Benedict's talk contained no explicit directive to the school presidents, but emphasized a core theme of his pontificate: that faith is compatible with reason.
"Teachers and administrators, whether in universities or schools, have the duty and privilege to ensure that students receive instruction in Catholic doctrine and practice," Benedict said. "Divergence from this vision weakens Catholic identity and, far from advancing freedom, inevitably leads to confusion, whether moral, intellectual or spiritual."
The speech was one of the most highly anticipated presentations of Benedict's six-day visit to the U.S. - his first since he was elected in 2005.
The nation's more than 200 Catholic colleges and universities have been at the center of a tug-of-war within the church for decades over religious identity and free expression.
Conservatives often criticize the colleges, accusing them of abandoning faith to conform to an increasingly secular world. Some of the most traditional Catholics have responded by building new, more orthodox schools. One of the best known is Ave Maria University in Florida, funded by Thomas S. Monaghan, founder of Domino's Pizza.
Nearly all American Catholic colleges and universities are independent, but local bishops provide spiritual guidance to the institutions.
In 2004, the U.S. bishops warned schools against honoring or giving a platform to Catholic lawmakers who support abortion rights and take other stands contrary to church teaching.
San Antonio Archbishop Jose Gomez complained after Democrat Hillary Rodham Clinton, who supports legal abortion, held a campaign rally in February at St. Mary's University.
Pope John Paul II had tried to strengthen Catholic identity on campus, partly by requiring a "mandatum" from U.S. Catholic theologians by 2002, pledging that they would teach authentic doctrine.
Many professors said it was a violation of academic freedom. Some U.S. bishops said they would not enforce the mandate. The process was private, and it is not known how many professors signed on.
The Rev. John Jenkins, president of the University of Notre Dame, said he appreciated the pope's message that Catholic educators "shouldn't make any untruth appealing or attractive."
He said Catholic colleges and universities already do that by distinguishing between "providing a forum where various views can be expressed and promoting views."
Nicholas Healy, president of Ave Maria University, said he was surprised that the speech had no specific prescriptions for how schools should uphold the faith.
"My guess is that if he had been legalistic in describing that certain schools had not met certain standards, it would not have had nearly the impact this will have over time," Healy said. "This is now a new paradigm for Catholic education in the 21st century. I think many schools are going to have to take a hard look to see whether they are following it."
Benedict, the Vatican's longtime doctrinal watchdog before he became pope, had played a key role in trying to bring Catholic colleges and universities in line with Rome.
As pontiff, his position on faith and education has met with some resistance.
In January, the Vatican took the rare step of canceling a visit by the pope to Europe's largest university, the public La Sapienza in Rome, following protests by a small group of students and professors, who depicted Benedict as opposed to science.
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AP Religion Writer Rachel Zoll contributed to this story.
