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In the 1970s and 1980s, the NFL solidified its dominance as America's top spectator sport,[citation needed] and its important role in American culture. The Super Bowl became an unofficial national holiday and the top-rated television program most years. Monday Night Football, which first aired in 1970, brought in high ratings by mixing sports and entertainment. Rule changes in the late 1970s ensured a fast-paced game with much passing to attract the casual fan.

The World Football League was the first post-merger challenge to the NFL's dominance, and in 1974, successfully lured some top NFL talent to its league and prompted a few rules changes in the NFL. However, financial problems led the league to fold halfway through its 1975 season. Two teams, the Birmingham Vulcans and Memphis Southmen, made unsuccessful efforts to move from the WFL to the NFL.

The founding of the United States Football League in the early 1980s would prove to be the longest sustained challenge to the NFL's dominance since the 1970 merger, lasting three seasons. The USFL was a relatively well-financed competitor with big-name players and a national television contract, but overspending on that talent and a decision to move its niche spring operation into a head-to-head competition with the NFL in the fall (abandoning some of its biggest cities in the process) over the objections of many of its original owners were two major factors in the league's demise. The league's last-ditch effort to sue the NFL for hundreds of millions of dollars in antitrust damages, while a technical victory, failed to secure the funds the USFL needed to survive.

The XFL was established in 2001 as an attempt by Vince McMahon and NBC, which had lost the NFL broadcast rights for that year, to compete with the league; the XFL folded after just one season. Unlike the WFL and USFL, the XFL had no impact on the NFL's rules or franchise locations, but a few NFL players used the XFL to relaunch their careers, and the league, while still considered a failure, has been reassessed in the 2010s and earned some greater respect for its attempt at integrating sports entertainment and innovative presentations into professional football. McMahon relaunched the XFL in 2020.

Prior to the 2002 season, the league realigned the divisions. The realignment consisted of eight divisions of four teams each. The NFC and AFC Central were renamed the NFC and AFC North, and the NFC and AFC South were created as brand new divisions. Arizona and Seattle join the NFC West, with Arizona leaving the NFC East and Seattle leaving the AFC West. Atlanta, New Orleans, and Carolina move from the NFC West to the new NFC South, along with Tampa Bay leaving the old NFC Central to join the NFC South. Jacksonville and Tennessee move from the old AFC Central to join to the new AFC South, along with Indianapolis moving from the AFC East to the AFC South. The other team to join the AFC South is the brand new expansion franchise Houston Texans. This realignment marked the first time the divisions were realigned in the league since the AFL-NFL merger in 1970.

The United Football League, which began play in 2009, had originally planned to take a direct challenge to the NFL with NFL-comparable salaries and teams in New York City and Los Angeles, but the UFL never did play in those cities (an ostensibly New York team played in Long Island and New Jersey), cut back its salaries, and instead opted for a complementary approach with teams in cities such as Las Vegas, Sacramento and Omaha; after four years, the UFL folded due to massive financial losses. Numerous other leagues have attempted to form over the years, but none have succeeded in having any level of competition comparable to the NFL (most never made it to their first game).

On August 31, 2007, a story in USA Today unveiled the first changes to the league's shield logo since 1980, which took effect with the 2008 season. The redesign reduced the number of stars in the logo from 25 (which were found not to have a meaning beyond being decorative) to eight (for each of the league's divisions), repositioned the football in the manner of the Vince Lombardi Trophy, and changed the NFL letters to a straight, serifed font. The redesign was created with television and digital media, along with clothing, in mind. The shield logo itself dates back to the 1940s.