In September, he signed a clothing deal with Puma. In the same month, he was also chosen as a captain's pick for the U.S. Ryder Cup team. At age 21 years and 9 months when the matches began, Fowler became the youngest U.S. Ryder Cup player of all time, and only European Sergio García was younger when he made his Ryder Cup debut in 1999. Fowler forfeited a hole during foursomes competition on the first match day because of a rules violation, by taking a permissible free drop from muddy conditions in an improper location, a mistake U.S. captain Corey Pavin attributed to Fowler's inexperience. On the final day of the competition in his singles match against Edoardo Molinari, Fowler birdied the last 4 holes to halve the match after having been 4 down after 12 holes.
While serving a suspension, Lowry signed a two-and-a-half-year permanent deal to Millwall for an undisclosed fee on 27 January 2012. Lowry then made his first appearance for the club since joining Millwall permanently, playing 90 minutes, in a 2–1 loss against rivals' West Ham United on 4 February 2012. Right way through March, Lowry was sidelined with ankle injury that kept him out for weeks. After making his first team return against Cardiff City, in a 0–0 draw on 31 March 2012, Lowry scored his first Millwall goal, which he scored the only goal in the game, in a 1–0 win over Coventry City on 17 March 2012. Lowry finished his 2011–12 season, making twenty-two appearance and scoring once.
On 23 November 2011, Lowry was again loaned out to play in the Championship, this time to Millwall until 3 January 2012. He followed Aston Villa team-mate Nathan Baker who also signed on loan for Millwall two days earlier. Lowry made his Millwall debut three days later, where he played 90 minutes, in a 0–0 draw against Crystal Palace. His impressive display at Millwall soon earned a loan extension. Weeks later on 13 January 2012, Lowry was sent-off in the 22nd minutes after stamping on Nikola Žigić, which saw Millwall lose 6–0. Three years on after signing for Birmingham City, Lowry stated, quoting: "Whatever club I play for I fully commit to that club at the time. I play with my heart on my sleeve. Sometimes in the past I have gone overboard but I was a younger player then, I have learned a lot from these types of experiences. But I am an aggressive player, that’s the way I like to play and I can’t change the way I play. I will use my experience now and be a bit more clever."'
After a T-12 finish at the Masters, Fowler earned his first win in over three years with a playoff victory at The Players Championship in May. Trailing Sergio García midway through the final round by five shots, Fowler played the final six holes in 6-under par, including an eagle at the par-5 16th. After a birdie at the famous 17th hole, Fowler's final birdie of the round on 18 left him at 12-under par. Both García and Kevin Kisner had birdie attempts to win at the 18th in regulation, but both missed and the three men went to a three-hole aggregate playoff to decide a winner on holes 16–18. Fowler and Kisner went par-birdie-par to tie at −1 while García's three pars left him at even and he was eliminated. Thus Fowler and Kisner went to sudden death starting at the 17th, where Kisner's tee shot landed within about 12 feet (3.7 m) of the cup. Fowler answered with a shot inside of five feet, and when Kisner's birdie attempt slid by, Fowler responded by making his short birdie to claim the championship. Fowler played his final 10 holes in 8-under par. On July 12, he won the Aberdeen Asset Management Scottish Open on the European Tour, shooting a 12-under-par 268. On September 7, he won the Deutsche Bank Championship, the second FedEx Cup Playoffs event, by one stroke over Henrik Stenson, for his third victory on the PGA Tour.
On June 16, Fowler carded a round of 65 at Erin Hills to take the first round lead at the 2017 U.S. Open. Fowler equaled the lowest first round score at the U.S. Open and led by one stroke from Paul Casey and Xander Schauffele. He followed this up with a one over par 73 in the second round to fall out of the lead by one stroke, held by four other players. He shot 68-72 over the weekend to finish in a tie for fifth place. This gave Fowler his sixth top-5 finish in a major, but he is still yet to win. Fowler started the PGA Championship with a 2-under 69 which was two strokes behind the leaders. After rounds of 70-73, he closed out the year's last major with a 4-under 67, including a run of four consecutive birdies on holes 12 through 15. Despite his solid finish, Fowler ended up tied for fifth and was 3 strokes behind the winner, and friend, Justin Thomas. It was his seventh top-5 major finish, meaning he's had multiple top-5 finishes at every major.
OHL Classic at Mayakoba: Birdied two of his last three holes at the OHL Classic at Mayakoba to fire a final-round 67 and finish in 2nd place, one shot back of Patton Kizzire. In his first start at the event, opened with a bogey-free, 6-under 65 to sit three back of Kizzire's lead. Followed with three-consecutives rounds of 67 in rounds two through four, resulting in a score of 18-under 266. Due to inclement weather Saturday, played his final two rounds on Sunday.
Hyundai Tournament of Champions: Finished T6 in a Monday-start-Tuesday-finish event, the season-opening, 54-hole Hyundai Tournament of Champions. The event "started" twice during the regularly scheduled first round Friday and later Sunday, but both times PGA TOUR rules staff halted play due to unplayable windy conditions and subsequently voided all scores that had taken place. As the first player off the tee, he ended up hitting three "opening" shots of the season.