The 47-year-old was a central figure in the recruitment process that led to Gareth Southgate's appointment as Sam Allardyce's successor.
Ashworth will join Brighton in 2019 and, alongside England's run to the semi-finals of the 2018 World Cup, he leaves an impressive legacy at St George's Park.
England's Under-20 and Under-17 sides won their respective World Cups in 2017, with the Under-19 squad tasting glory at the European Championship in the same year.
"Having recently attended a FIFA conference with Dan, we walked in the room as semi-finalists at a major tournament for the first time in 28 years but perhaps even more significantly as world champions at Under-17 and Under-20 level," Southgate said in an FA statement.
"In terms of the work of a technical director, I don't think he could have had a bigger impact with the plans he put in place at the FA and the way that the national teams have progressed in the time Dan has been in charge.
"That's coupled with the transition into St George's Park and the outstanding staff structure he's put in place. I think he can be really proud."
In a Brighton statement, Ashworth said: "I am delighted to be joining Brighton and Hove Albion, one of the country's most progressive clubs.
"The success we have had with our national teams is down to careful planning and high performance from the players, but also the hard work and professionalism of a lot of people over a sustained period of time, and of course the relationship we have had with the clubs, the leagues and the national game."It's been an honour and great pleasure to serve my country in the past half-decade."