After being involved in the Los Angeles drug subculture and kicked out of high school, Eldredge was looking for a "worldview." After exploring other religions, Eastern mysticism, Lao-Tzu, and New Age spirituality, he discovered the writings of Francis Schaeffer, whom he calls one of the best philosophers of the 20th century. Through Schaeffer, Eldredge came to Christ and later to the church. He eventually got a master's degree in counseling and practiced in Colorado Springs before working for Focus on the Family.

John received his undergraduate degree in theater from California Polytechnic University (Pomona) and his MA in biblical counseling from Colorado Christian University under the direction of Dr. Larry Crabb and Dr. Dan Allender. Prior to joining Focus on the Family in 1988, John served for five years on the staff of Sierra Madre Congregational Church in Southern California.

In July 2000, John left Focus on the Family to launch Ransomed Heart Ministries, a ministry devoted to furthering the message of his book The Sacred Romance. A sought-after speaker, John travels extensively in the U.S. and abroad. John, his wife, Stasi, and their three sons live in Colorado Springs, Colorado.

Some passages in Eldredge's books have caused leaders in other churches to question the perspective that defines Eldredge's style. As an example, Christianity Today quotes Rut Etheridge III, a seminarian in the Reformed Presbyterian Church of North America, who describes Eldredge as having an "alarmingly unbiblical worldview."

Eldredge uses descriptive language and gives references to popular culture in his writing more so than to substantive theories and quantitative studies. As an example, Eldredge says that "Contrary to what you may have been led to believe, the Incarnation of grace, meekness, and love is not Mister Rogers with a beard! He is more like Maximus in the movie Gladiator or William Wallace in Braveheart." Eldredge's references to Gladiator and Braveheart have also been criticized as part of his portrayal of Christian masculinity being focused on warfare and violence.

Although he does not promote criminality, Eldredge has also received criticism for use made of his book Wild at Heart by the "pseudo-evangelical cult" and Mexican criminal cartel La Familia Michoacana.