The stadium's re-opening day was also the home debut of the Jaguars during the 1995 NFL season. It was the first time that an expansion NFL team had played its first game in a new facility; they played the Houston Oilers in the opener and lost 10–3. The Gator Bowl returned as a New Year's Day bowl game on January 1, 1996, following the 1995 NCAA season.

The stadium contains 11,200 club seats, 88 luxury suites, and a "super suite".

In 1997, the stadium changed its name to Alltel Stadium after naming rights were acquired by Alltel, a telecommunications company best known as a wireless carrier. The name Alltel Stadium stopped being used by the city after January 2007 when the contract expired; by that point, most of Alltel's assets had been purchased by Verizon.

In 2005, the stadium hosted Super Bowl XXXIX in which the New England Patriots defeated the Philadelphia Eagles 24–21 in front of 78,125, the largest Super Bowl in attendance since 1994. Paul McCartney performed at halftime, performing Beatles classics "Drive My Car", "Get Back", and "Hey Jude", as well as a firework-filled "Live and Let Die". In 2003 and 2004, $47 million in improvements to the stadium were implemented to prepare for the Super Bowl. These improvements included the addition of a unique sports bar in the south end zone called the "Bud Zone", a larger and wider video and scoring display from Daktronics, escalators in the north and south end zone, and a new "terrace suite" called the "Sky Patio" right above the "Bud Zone" in the south end zone.

Before the 2005 season, mainly due to low attendance figures and looming blackouts, team officials installed a series of tarps to reduce the seating capacity for Jaguars games. The covers were placed to block out seven sections in the upper north end zone and four in each upper deck section, located on the corners of each. This puts 9,703 seats out of service, leaving the stadium with 66,851 seats for the regular season. However, in the event the Jaguars make the AFC Championship Game, the stadium can easily be expanded to full capacity. Some believed that this was a sign that the city couldn't support an NFL team; the city is the second-smallest market in the league. However, the current capacity is actually very close to what Wayne Weaver included in his original proposal to bring the Gator Bowl up to NFL standards. The city council turned this plan down, mainly out of concern for not having enough seats to accommodate the annual Florida-Georgia game.

Despite the changes, however, blackouts have still occurred, including two of their first three home games in 2007 and nine of ten games in 2009. It is believed that the 2008 US financial crisis played a major part in the 2009 season blackouts, leading to insufficient ticket sales, with only the final home engagement of the regular season, with the Indianapolis Colts, managing to sell out. However, the Jaguars' 2010 season saw a huge turnaround in ticket sales, with no games being blacked out that year. The Jaguars avoided blackouts in all games in 2011 and 2012.

For the Super Bowl, Florida–Georgia game, and occasionally the Gator Bowl, temporary bleachers are put up in the south end zone and the tarps are removed, raising capacity to over 84,000.

The attendance record was set on September 29, 2007, when 85,413 watched Florida State defeat Alabama in what was dubbed the River City Showdown. Each school received nearly 36,000 tickets, and the Gator Bowl Association added 5,800 seats.

On July 26, 2010, naming rights to the stadium were bought by EverBank, one of the nation's largest privately held bank holding companies with approximately $11.2 billion in assets. On August 10, the deal was officially approved by the Jacksonville City Council with a 14–3 vote.

In November 2013, Jacksonville's City Council approved $63 million in improvements to EverBank Field. Jaguars owner Shahid Khan helped finance $20 million of the cost. Renovations included two end zone video scoreboards 362-foot (110 m) long that are the largest HD LED of their kind in the world, a platform area in the north end zone with two wading pools, unique food and beverage offerings, interactive activities, and 55,000 square feet (5,100 m2) of HD video screens, which is a world record for a stadium. Construction of the platform resulted in the removal of approximately 7,000 seats, though temporary seating can be installed for major events that will require a larger stadium capacity. During the construction a live webcam was set up to view the progress of the new video scoreboards. The scoreboards were publicly unveiled on July 26, 2014.

In the middle of 2016, the Jaguars and the city of Jacksonville announced $90 million in improvements to the stadium. Phase 1 includes the improvements to club seating, sponsored by US Assure, new walkout patios at the 50-yard-line and the creation of a new south end zone tunnel that will be the new team entrance and create two new seating environments. Phase 2 includes the construction of an amphitheater (Daily's Place) and a covered flex field; both phases were completed in May 2017.

After the successful 2017 season which saw the Jaguars return to the playoffs for the first time since the 2007 season and host a playoff game for the first time since 1999, the Jaguars announced the removal of last of the tarps on the upper levels. The removal adds 3,501 seats to the capacity of the stadium bringing total capacity to 67,814.

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