Coughlin was also the inaugural head coach of the Jacksonville Jaguars, serving from 1995 to 2002 and leading the team to two AFC Championship Game appearances.

Coughlin's success at Boston College led to his subsequent hiring as the first head coach of the NFL's expansion Jacksonville Jaguars.

The first time, in only the second year of the team's existence (1996), the Jaguars qualified for the playoffs on the last day of the season and upset the heavily favored Buffalo Bills and Denver Broncos on the road.

In 2011, after selling the Jaguars to Shahid Khan, Weaver said when looking back on his tenure as owner, one of his biggest regrets was firing Coughlin.

Coughlin's incumbent quarterback, Kerry Collins, was incensed by the move and demanded his release, leaving the team without a veteran who could hold the fort until Manning was ready.

To fill that role the Giants signed Kurt Warner, the former league MVP who had been cut by the St. Louis Rams after he lost his starting job to Marc Bulger.

However, with the team losing their next two, Coughlin decided that Warner, who had been struggling, could no longer do the job and began starting the highly-touted Manning beginning in the tenth game.

The coach received criticism from some who felt the move amounted to a surrender of the 2004 season; their 5–4 record meant the Giants were still in playoff contention.

Barber also saw his production increase significantly, setting career highs in rushing and total yards each year under Coughlin.

After a particularly bad loss to the Seattle Seahawks, star tight end Jeremy Shockey stated that the Giants had been "outplayed and outcoached."

Things took another turn for the worse the next week when the Giants blew a 21-point fourth quarter lead and lost to the Tennessee Titans by a score of 24–21.

The Giants rebounded with a victory in the season's final game at the Washington Redskins, thereby securing a playoff berth and perhaps saving Coughlin's job in the process.

He cited numerous complaints about Eli Manning's leadership skills and Coughlin's practice style as decisions to retire at what seemed the peak of his career.

In the final seconds the Giants were faced with a fourth down and Coughlin told his punter, Matt Dodge, to punt the ball out of bounds to effectively end the game.

[18] Following a very hectic free agency period when the Giants lost Pro Bowl wide receiver Steve Smith, defensive tackle Barry Cofield, and tight end Kevin Boss, expectations from many analysts and fans alike were very low.

[22] In the 2011 divisional game Coughlin coached the Giants to a 37–20 win over the heavily favored defending Super Bowl XLV champion Green Bay Packers,[23] a team who finished the 2011 regular season with a league best 15–1 win–loss record.

The following week, he coached the Giants to a 20–17 overtime victory over the San Francisco 49ers in the NFC Championship Game to set up a Super Bowl rematch with the New England Patriots.

This was due in large part to two lopsided losses to the NFC's number one seed Atlanta Falcons and eventual Super Bowl XLVII champion Baltimore Ravens in weeks 15 and 16 respectively.

[30] Despite the difficult start, the team remained resilient and rebounded with wins against the Minnesota Vikings and Philadelphia Eagles,[31][32] hitting the bye week at 2–6.

Victories against the Oakland Raiders and Green Bay Packers,[33][34] coupled with a floundering NFC East, left the Giants only one and half games behind the division-leading Eagles going into week 12.

Criticism of Coughlin built throughout the season and peaked in Week 15, after a 38–35 loss to the eventual NFC champion Carolina Panthers in which Coughlin left star receiver Odell Beckham Jr. in the game despite Beckham's on-field behavior, including numerous scuffles with Panthers cornerback Josh Norman, resulting in a slew of personal foul penalties.

In a statement released by the Giants that day, Coughlin wrote, "I met with John Mara and Steve Tisch this afternoon, and I informed them that it is in the best interest of the organization that I step down as head coach.

However, he reportedly decided to oust Coughlin right away after the NFL Players Association announced it had won a grievance filed by linebacker Dante Fowler, now of the Dallas Cowboys.

Fowler contended that the Jaguars had improperly fined him a total of $700,000 for not attending rehab and medical appointments in Jacksonville during the 2018 offseason that should have been optional under the collective bargaining agreement.

The NFLPA took the unusual step of publicly warning free agents against signing with the Jaguars because of Coughlin's reported disregard for player rights.

[49] Tim survived the 9/11 terrorist attacks, successfully evacuating his South Tower 60th floor office at Morgan Stanley.

[53] In January 2017, it was revealed that Coughlin had been re-hired by the Jacksonville Jaguars to be the team's executive vice president for football operations.

[55] On July 30, 2020, Coughlin broke four ribs, punctured a lung, and needed stitches on his head, after a getting into a biking accident with a fellow biker.

The foundation is named after Jay McGillis, a Boston College player who had been diagnosed with and died from leukemia during Coughlin's tenure as head coach.

The non-profit organization is devoted to assisting "children with leukemia and other cancers and their families by providing emotional and financial support to help reduce the stress associated with treatment and improve their quality of life", according to the foundation's mission statement.