Girmay started his sprint early with Van der Poel (Alpecin-Fenix) following, but the Dutchman was unable to come around and match the Eritrean's speed, sitting up before the line and giving him a thumbs-up in a moment of respect between the competitors.
Vincenzo Albanese (Eolo-Kometa) was the next to finish in third along with the rest of the bunch, containing most of the overall contenders as the general classification remained unchanged, Juan Pedro Lopez (Trek-Segafredo) keeping the maglia rosa for another day.
The win saw Girmay flip the script on Van der Poel after they duelled in similar fashion on the opening stage, and the two were seen shaking hands following the finish.
“All the team was working all day, including the GC riders, and they did a great job,” Girmay said with a smile after the finish.
“We knew when we started we knew we had possibilities to win a stage.
I made history thanks to my team, my family, the support from the people of my country. This victory belongs to them also. I am thankful and happy that I was able to pay back the team for a win.”
The 196 kilometre stage from Pescara to Jesi saw the peloton resume after the second rest day with a pancake flat first 100 kilometres that saw a three-man break form with Lawrence Naesen (Ag2r-Citroën), Matti Bais (Drone Hopper), and Alessandro De Marchi (Israel-Premier Tech).
The trio never amassed a sizeable gap and were kept in the sights of the Alpecin and Intermarche-led peloton for the duration of the stage, Naesen and Bais gradually reeled in before De Marchi was the last to be caught with 20 kilometres remaining.
The second half of the stage brought hilly terrain that left some of the top sprinters unable to stay with the pack, including Caleb Ewan (Lotto Soudal), Mark Cavendish (QuickStep-Alpha Vinyl) and Arnaud Demare (Groupama-FDJ).
The final climb with 9 kilometres to go then saw numerous attacks from the reduced peloton, with Alessandro Covi (UAE Team Emirates) the first to go, gaps forming amongst the GC contenders as they were forced to chase him down.
The descent into the finish was then Vincenzo Nibali's (Astana Qazaqstan) turn to try a move before Van der Poel launched with 4.5 kilometres to go which also ultimately proved unsuccessful as no one was giving an inch.
With Van der Poel reeled in, Richard Carapaz (INEOS Grenadiers) attacked to put the GC under pressure once again, everyone battling hard to regroup and get in position for the run to the finish.
With 600 metres to go, Girmay launched off the wheel of teammate Domenico Pozzovivo with serious power, Van der Poel the only one to follow with the pair again stronger than the rest of the bunch.
As the line got closer, the Dutchman appeared to be almost alongside Girmay, but reached his limit allowing the Eritrean to ride through for an emphatic celebration.
The Giro d'Italia continues tonight with Stage 11, a pancake flat 203 kilometre ride through the region of Emilio-Romagna that may be Caleb Ewan's best remaining chance for victory. Watch the action from 7:20pm AEST on SBS On Demand, with the SBS broadcast starting at 11pm AEST. WA viewers can tune in from 9pm AWST on SBS VICELAND.
