This Colts team, now in the "big league" of professional American football for the first time, although with shaky financing and ownership, played only in the 1950 season of the NFL, and was later disbanded.

In 1953, a new Baltimore-based group, heavily supported by the city's municipal government and with a large subscription-base of fan-purchased season tickets, led by local owner Carroll Rosenbloom won the rights to a new Baltimore NFL franchise.

The result of the game surprised many in the sports media[18] as Joe Namath and Matt Snell led the Jets to the Super Bowl victory under head coach Weeb Ewbank, who had previously won two NFL Championships with the Colts.

[8] The Colts immediately went on a rampage in the new league, as new head coach Don McCafferty led the 1970 team to an 11–2–1 regular-season record, winning the AFC East title.

[21] Citing friction with the City of Baltimore and the local press, Rosenbloom traded the Colts franchise to Robert Irsay on July 13, 1972, and received the Los Angeles Rams in return.

[23] These consecutive championship teams featured 1976 NFL Most Valuable Player Bert Jones at quarterback and an outstanding defensive line, nicknamed the "Sack Pack".

The Maryland General Assembly intervened when a bill was introduced to give the city of Baltimore the right to seize ownership of the team by eminent domain.

[32] After the deal was reached, moving vans from Indianapolis-based Mayflower Transit were dispatched overnight to the team's Maryland training complex, arriving on the morning of March 29, 1984.

[36] The 1985 and 1986 teams combined for only eight wins, including an 0–13 start in 1986 which prompted the firing of head coach Rod Dowhower, who was replaced by Ron Meyer.

The Colts, however, did receive eventual Hall of Fame running back Eric Dickerson[37] as a result of a trade during the 1987 season, and went on to compile a 9–6 record, thereby winning the AFC East and advancing to the postseason for the first time in Indianapolis; they lost that game to the Cleveland Browns.

[46] Along with the disappointing season, the principal owner and man who moved the team to Indianapolis, Robert Irsay, died in January 1997 after years of declining health.

[48] Jim Irsay began to shape the Colts one year after assuming control from his father by firing head coach Lindy Infante and hiring Bill Polian as the general manager of the organization.

[59] Dungy and the team quickly changed the atmosphere of the organization and returned to the playoffs in 2002 with a 10–6 record, only for them to get shut out in the 2002 Wild Card Round to the New York Jets.

[95] The Colts also began to release some higher paid and oft-injured veteran players, including Joseph Addai, Dallas Clark, and Gary Brackett.

[125] Colts General Manager Chris Ballard achieved a historic feat in 2018 when two players he had drafted that year, guard Quenton Nelson and linebacker Shaquille Leonard were both named First-Team All-Pro.

[130] On March 17, 2020, the Colts signed longtime Los Angeles Chargers quarterback and eight-time Pro Bowler Philip Rivers to a one-year deal worth $25 million.

[137] After playing seven games in which he threw for nine touchdowns and nine interceptions, while also fumbling 11 times, Ryan was benched for the remainder of the season in favor of Sam Ehlinger.

[149] Despite many injuries, including to Richardson and All-Pro running back Jonathan Taylor, the 2023 Colts rebounded from their 4–12–1 record in 2022, finishing 9–8 and narrowly missing the playoffs with a loss to the Houston Texans in the season finale.

[160] In December 2004, the City of Indianapolis and Jim Irsay agreed to a new stadium deal at an estimated cost of $1 billion (including the Indiana Convention Center upgrades).

Despite Indianapolis dominating the AFC South and this particular series under quarterback Peyton Manning in the 2000s, Houston has recently provided more competition, winning the division five times since 2011.

Although the Jaguars have struggled to maintain a consistently competitive roster, they have managed to achieve significant upsets against the Colts[168][169][170] and have recorded more victories against them than against the Titans and Texans.

[189] In the years 1953–66, the Colts played in the NFL Western Conference (also known as division), but did not have significant rivalries with other franchises in that alignment, as they were the easternmost team and the rest of the division included the Great Lakes franchises Green Bay, Detroit Lions, Chicago Bears, and after 1961, the Minnesota Vikings, along with the league's two West Coast teams in San Francisco and Los Angeles.

[192] Super Bowl III became the most famous upset in professional sports history as the American Football League's New York Jets won 16–7 over the overwhelmingly favored Colts.

Unitas threw for 376 yards and two scores but was sacked six times as the Jets won 44–34; the game was considered one of the top ten passing duels in NFL history.

[195] Baltimore's post NFL-AFL merger passage to the AFC saw them thrust into a new environment with little in common with its fellow divisional teams: the Jets, Miami Dolphins, Buffalo Bills, and Boston Patriots.

The two franchises were denied a playoff confrontation by Miami's first-round defeat to the Oakland Raiders, whereas Baltimore won its first Super Bowl title that year.

In the playoffs, Baltimore advanced to the AFC title game after a 20–3 victory over the Cleveland Browns, while Miami won in double overtime against the Kansas City Chiefs.

The rivalry was effectively retired after this; the two clubs did meet in a memorable Monday Night Football matchup in 2009 where the Colts, despite having the ball for only 15 minutes, defeated the Dolphins 27–23.

The team's local TV carriage rights were shaken up in mid-2014 when WTTV's owner Tribune Media came to terms with CBS to become the network's Indianapolis affiliate as of January 1, 2015, replacing WISH-TV.

[225] With the deal, both Tribune Media stations, including WXIN (channel 59) carry the bulk of the team's regular-season games starting with the 2015 NFL season.