Following nearly three decades of unsuccessfully trying to gain an expansion franchise or enticing existing teams to relocate to the Tampa Bay area, an ownership group led by Vince Naimoli was approved on March 9, 1995.

The Oakland A's, Minnesota Twins, Chicago White Sox, Texas Rangers, Kansas City Royals, and Seattle Mariners all seriously considered moving to either Tampa or St. Petersburg, but they all elected to remain in place, usually with the enticement of a new publicly-funded ballpark.

[9][10] In response, the city of St. Petersburg decided to build the Florida Suncoast Dome (now called Tropicana Field) in the mid-1980s for the express purpose of luring a major league team with a move-in ready facility.

[11][page needed] When MLB announced plans to add two expansion teams for the 1993 season, it was widely assumed that one would be placed in the Tampa Bay area, most likely St. Petersburg.

Naimoli initially planned to call the team the "Tampa Bay Sting Rays" but the naming rights were already held by the minor league Maui Stingrays.

Despite the change, the team continued to decline, and the 2002 season would lead to a franchise-worst 55–106 record, despite the emergence of key players like Aubrey Huff, Toby Hall, and Carl Crawford.

The next year, Piniella's Devil Rays finished with a 70–91 record, just above the Toronto Blue Jays to claim in 4th in the American League East—the first time in franchise history the team was out of last place.

In the 2005 season, Crawford's production at the plate was matched by newcomers Jorge Cantú and Jonny Gomes, though the team was let down by its pitching staff (despite the arrival of Scott Kazmir) and finished 67–95.

[30] The Rays briefly fell behind the Boston Red Sox but, with the best home record in Major League Baseball, manage to qualify for at least the AL Wild Card on September 20—the team's first-ever postseason berth.

Going into the 2009 season, the American League champions again posted a winning record, 84–78, but were unable to return to the postseason, in part due to injuries to Longoria, Akinori Iwamura and Carlos Peña.

The Rays lost veterans like Garza, Peña, and Crawford in the 2010–11 offseason, but nevertheless finished the 2011 season with the AL wild card, having just barely beat out the Red Sox with a 12th-inning walk-off home run by Evan Longoria against the Yankees.

The team fared more poorly in the next year; they finished last in the AL East for the first time since 2007, winning only 68 games in a season marred by injuries (including to Kiermaier) and a 3–24 stretch between June 16 and July 16.

The roster would change even more after opening day; Willy Adames was traded to the Milwaukee Brewers and Glasnow underwent Tommy John surgery that would place him on the injured list through 2022.

Tampa Bay hosted the eventual world champion Texas Rangers in another two-game Wild Card loss where the Rays never led at any point with just one run scored yet again.

[48] The Red Sox/Rays rivalry dates back to the 2000 season, when Devil Ray Gerald Williams took exception to being hit by a pitch thrown by Boston pitcher Pedro Martínez and charged the mound, resulting in a game full of retaliations and ejections on both sides.

[49] There have been several other incidents between the teams during the ensuing years, including one in 2005 that resulted in two bench-clearing fights during the game and a war of words between then-Devil Rays manager Lou Piniella and then-Boston pitcher Curt Schilling through the media in the following days.

[50] The rivalry reached its highest level to date during the 2008 season, including a brawl during a June meeting in Fenway Park[51] and a seven-game American League Championship Series between the teams that ended in the Rays' first ever pennant win.

There has always been some feeling of a rivalry between the teams because the Yankees make Tampa their spring training home, as well as having a minor league team in the Tampa Tarpons; home and fan loyalty in the Tampa Bay area has historically been divided, especially among transplants from the northeastern U.S.[52] The rivalry became more heated in spring training of 2008, when a home plate collision between Rays outfielder Elliot Johnson and Yankees catcher Francisco Cervelli was followed the next day by spikes-high slide by Yankees outfielder Shelley Duncan into Rays' second baseman Akinori Iwamura, prompting Rays outfielder Jonny Gomes to charge in from his position in right field and knock Duncan to the ground.

On November 14, 2024, the Rays announced that the team will play the 2025 regular season at George M. Steinbrenner Field in Tampa, the spring training home of the New York Yankees.

The Rays stadium, Tropicana Field in St. Petersburg, was significantly damaged by Hurricane Milton on October 9 and will not be available when the team opens the regular season in late March.

[59] The Rays' current ownership has stated that Tropicana Field does not generate enough revenue, and that its location in St. Petersburg is too far from the Tampa Bay area's primary population center in Hillsborough County.

[61] In 2007, the team announced a plan to build a covered ballpark at the current site of Al Lang Field on the St. Petersburg waterfront, and a local referendum was scheduled to decide on public financing.

[63] However, in the face of vocal opposition, the Rays withdrew the proposal in 2009 and stated they had abandoned all plans for a ballpark on the downtown St. Petersburg waterfront, preferring a location nearer to the center of Pinellas County or across the bay in Tampa.

[65] However, St. Petersburg mayor Bill Foster repeatedly insisted that the Rays honor their use agreement with the city, which runs through 2027 and prohibits the team from entering into talks with other communities, resulting in a protracted stalemate.

[71] However, at the December 2018 Winter Meetings in Las Vegas, Sternberg announced that plans for the proposed stadium in Ybor fell through, meaning the Rays were still on track to play at Tropicana Field until 2027.

[79] Team president Matt Silverman announced the Rays' intention to display a "Tampa Bay/Montreal" graphic in the right field foul territory at Tropicana Field during the 2021 MLB postseason to promote the team's split-city concept for the future,[80] although those plans were dropped shortly after alongside an apology from owner Stuart Sternberg, who said he made "a real mistake, in trying to promote our sister-city plan with a sign right now in our home ballpark".

[82] On September 19, 2023, the Rays announced that they plan to build a new ballpark in St. Petersburg adjacent to Tropicana Field as part of the redevelopment of the Gas Plant District and will open for the 2028 season.

They also changed the font on their jersey tops and shortened the name on the home whites to read simply "Rays" while keeping "Tampa Bay" on the road grays.

These uniforms were patterned after those of the San Diego Padres from the late 1970s, but with the Rays' name (including a circular yellow sunburst) and team colors of gold, navy, and powder blue.

DJ Kitty was introduced in 2010, initially through a video that would play on the scoreboard whenever the game situation called for a rally, in which a large anthropomorphic cat, wearing a Rays jersey, appeared on the screen wielding a turntable similar to those used by rap DJs.