Two days after the Three Lions came up just short yet again -- losing the Euro 2024 final to Spain -- the 53-year-old has stepped down, deciding it is time for a "new chapter".
The mild-mannered Southgate transformed England into a consistent force on the international stage after decades of under-achievement.
He also reshaped the team culture, breaking down barriers that had previously existed within the camp between players from rival clubs.
But he ultimately failed to end the nation's long wait for a major trophy dating back to Alf Ramsey's 1966 World Cup victory despite having a richly talented generation of players to work with.
Humiliations
Southgate took over with England at a low ebb after a series of humiliations on and off the pitch.
A woeful Euro 2016 exit against Iceland brought a suitably depressing end to Roy Hodgson's reign, while his successor, Sam Allardyce, lasted only 67 days and one match before being forced out after a newspaper sting.
Southgate, short of top-level managerial experience, gained credibility among previously sceptical fans with a surprise run to the 2018 World Cup semi-finals in Russia.
The diffident boss even became a style icon back home as sales of his trademark waistcoat soared.
He followed that impressive achievement by leading England to their first major final for 55 years at the Covid-delayed European Championship in 2021, where they lost on penalties to Italy.
England went out to eventual finalists France in the quarter-finals in Qatar in 2022 but there were still positive signs that this was a young and exciting team heading in the right direction.
Southgate's men were among the favourites to finally get over the line at Euro 2024 but it turned into a roller coaster of emotions for the manager, who went from having beer cups thrown at him to within touching distance of winning the cup in Berlin.
England only gelled sporadically but produced enough individual moments of brilliance to go all the way to the final.
Jude Bellingham's moment of magic with a bicycle kick deep into stoppage time against Slovakia in the round of 16 allowed Southgate to bring up his 100th match in charge against the Swiss.
But it also served as a reminder of the quality of player at his disposal.
A squad containing Real Madrid's Bellingham, Bundesliga top-scorer Harry Kane and the Premier League's player of the year Phil Foden ultimately proved to be less than the sum of its parts.
Penalty pain
Southgate, in his resignation statement on Tuesday, said it had been the "honour of my life to play for England and to manage England".
He was stung by the vitriol aimed at him by some fans in Germany, admitting "we all want to be loved" after England beat the Netherlands 2-1 to reach the final.
Southgate tasted the highs and lows as a manager and as a player -- famously failing from the penalty spot in a semi-final shootout loss to Germany at Euro 1990.
He had only had one managerial job -- at Middlesbrough -- when in 2013 he was put in charge of the England Under-21 team.
But he stepped up from that role after the embarrassing Allardyce episode, filling the top job on a temporary basis.
The 57-cap former defender grasped the nettle and a promising four-game interim stint earned a permanent deal.
Despite England's success, criticism of his perceived lack of tactical nous and inflexibility has always simmered.
At Euro 2024 he was accused of being too cautious, of an unwillingness to allow his men to express themselves.
But he leaves an important legacy and a framework in place for a tilt at future honours.
"He's changed our culture within our team, which is extremely difficult with players coming from different club environments," said Manchester City defender John Stones.
"To feel so comfortable within everyone's company, on the pitch -- the humility, the winning mentality."
The next manager of England might finally take the side to the promised land, but he will owe a large debt to a man described by Prince William as an "all-round class act".
