His son-in-law, Chris Snee, currently plays for him on the Giants.

After he graduated from Waterloo High School, Coughlin attended Syracuse University where he played wingback and was teammates with Larry Csonka and Floyd Little. In 1967, he set the school's single-season pass receiving record. His first head coaching job was at the Rochester Institute of Technology from 1970-1973. After his success there, he returned to his alma mater where he was eventually promoted to offensive coordinator, a position he also held at Boston College where he coached Doug Flutie. He left the collegiate level to become a wide receivers coach in the NFL for the Philadelphia Eagles, and later the Green Bay Packers and New York Giants. While at New York he was an assistant to Bill Parcells, and helped the Giants win Super Bowl XXV.

After the season, Coughlin returned to Boston College to take on his first job as a head coach. During his time at BC, Coughlin became known as one of college football's great offensive minds. In three seasons at BC, he turned the program into a consistent winner. Coughlin's tenure was capped with an incredible 41-39 victory over #1 ranked Notre Dame in one of the great college games of all time. His success led to his subsequent hiring as the first head coach of the NFL's expansion Jacksonville Jaguars. In 8 seasons at Jacksonville, he helmed the most successful expansion team in league history, leading the Jaguars to the AFC Championship Game twice, the first time being only the second year of the team's existence, 1996, where he lost to Bill Parcells and the New England Patriots, but was named NFL Coach of the Year by United Press International.

After being out of football in 2003, Couglin was named the 16th head coach of the New York Giants on January 6, 2004. Not known as a player's coach, Coughlin is infamous for his tough, disciplined approach. In a 2004 Sports Illustrated poll of 354 current and former NFL players, Coughlin received 29% of the votes to the question, "Who is the worst coach in the league?", by far the most of any coach. He was also heavily criticized when he benched veteran quarterback Kurt Warner for rookie Eli Manning nine games into the 2004 season, especially after the Giants lost six out of seven games that Manning started that season. Despite the criticism, he refuses to change and the results are there for all to see. Coughlin was mentored by Bill Parcells, when he spent time as Wide Receivers Coach on the Giants, along with many other assistants who are currently Head Coaches in the N.F.L., and the two are close friends who face off in the NFC East. Recently Coughlin has gotten the upperhand, going 3-1 versus Parcells since he was hired by the Giants. The Giants finished Coughlin's second year as head coach with an 11-5 record, their first NFC East Division title since 2001, and their first playoff appearance since 2002, a vast improvement after experiencing two consecutive losing seasons. Perhaps the biggest improvement to the Giants under Coughlin has been the emergence of running back Tiki Barber as one of the premier players in the NFL since growing out of a bad tendency to fumble, which he credits Coach Coughlin with curing. Tiki was recently selected to the Pro Bowl for the second consecutive year, an accolade he never attained prior to Coughlin's arrival. The Giants have also gotten more out of their draft selections and free agent signings since Coach Coughlin's arrival.