Dominic Dwyer joined Norwich's academy in June 2000 as a schoolboy. After playing for Staines Town and then Kings Lynn Reserves in the Ridgeons League, he signed conference terms with the Linnets on 29th August 2008

Dwyer left Lynn in the summer of 2009 take up a soccer scholarship at Tyler Junior College, Texas. He also coached in the local community on behalf of the university. He was named National Junior College Player of the Year in 2010 after leading his college to their second consecutive national championship.

He joined the University of South Florida in 2010 and scored 16 goals in 18 games. A successful season saw him asked to attend the MLS combine. The event is a chance for top university players to showcase themselves in front of professional coaches. And it was an opportunity the English ace grabbed with both hands impressing Sporting Kansas City enough to select him in the MLS Draft.

“It’s pretty unbelievable and I won’t ever experience anything like it again,” said Dwyer of the draft process – a selection feature of many American sports. “You’re kind of just sitting there with 19 teams that can choose you. You don’t know what team you’re going to be playing for or where you’ll be living, it’s pretty crazy. You’re also worried about thinking is anybody going to pick me? “I was told I was going to be picked at number three, then number seven, then 10, then 12, 14 and 15. I was kind of waiting and all these numbers kept passing on by and I was getting more worried. It was unbelievable to get picked in the end. I’d spoken to almost every team before the draft, except Kansas, which made it even more of a surprise.” He was also chosen as a Generation Adidas athlete, a joint venture between the MLS and US Soccer aimed at raising the level of young talent in the country

He only made a handful of competitive appearances in 2012 and spent much of last year in the shadows.Having trained with St Mirren at the end of the MLS season, Dwyer’s impending loan move to the Scottish Premier League was blocked. While fellow striker Kei Kamara was heading abroad to Norwich City on a short-term deal in the same month, his KC team-mate was being sent America to Orlando City on a season-long loan. The USL Pro outfit play in the third-tier of American football, England’s equivalent of League One. And Dwyer has wasted no time in showing that he’s arguably too good for that level. The frontman has already bagged an Orlando season-best record of 13 league goals in just 11 matches.

On 27th June 2013, Dwyer was recalled by Sporting Kansas City the morning following Orlando's US Open Cup defeat to Chicago Fire SC which saw Orlando eliminated from the competition. On 3rd August 2013, Dwyer scored first goal in MLS against the New York Red Bulls in the second minute of stoppage time.

On 8th August 2013, Dwyer made his debut in the CONCACAF Champions League for Sporting. In the 75th minute, he scored to give Sporting a 2–0 lead against Nicaraguan outfit, Real Esteli. Coming back for one more game with Orlando City on 7th September 2013, Dwyer scored four goals, a club record for one game, against the Charlotte Eagles in the 2013 USL Pro Championship final, leading the Lions to a 7-4 victory in front of a 20,000+ crowd.

Dwyer's 63rd minute goal against Houston Dynamo on 25th November 2013 won Sporting Kansas City a place in the MLS Cup Final. They beat Real Salt Lake 7-6 on pens in the final on 8th December 2013, with Dwyer starting the game as did goalkeeper Jimmy Nielsen.

Dwyer told the Telegraph in mid December that he was likely to join a Championship side on loan in January 2014, with a view to a permanent transfer. In January 2014, he joined Charlton on trial.

In July 2014, it was speculated that Dwyer might receive a call-up to the USA national team. He would be eligible to play for the USA from 2017. He also hit the headlines for running into the crowd and taking a selfie after scoring for Sporting Kansas City against the Chicago Fire. He received a yellow card. Later that summer, Brentford were linked with a move for Dwyer.

He received USA citizenship in March 2017 and was called into the USA squad in June 2017 for the Gold Cup. He made his international debut on 1st July 2017 against Ghana and scored after just 19 minutes in a 2-1 victory for the USA. Dwyer said “It’s been a long road to get here. I really wanted to show the fans and show the country that I’m very passionate about this country and that I’m very honoured to play for this team. Hopefully, it’s something we can build on.”

On 25th July 2017 Dwyer was signed by Orlando City in exchange for US$900,000 in guaranteed allocation funds (split between general and targeted), as well as up to US$700,000 in future allocation funds based on his performance. This made him the most expensive player in MLS history.

He was released by Orlando on 1st January 2021 having made 70 appearances for Orlando and scoring 24 goals to take his career total to 113 goals in 249 appearances.

On 11th May 2021 he signed for Toronto FC