Obama announced Verrilli's resignation in a statement Thursday. He'll be replaced by his principal deputy, Ian Gershengorn, who will take over as acting solicitor general on June 25, Attorney General Loretta Lynch said.
"For five years, Solicitor General Don Verrilli has fought in our nation's highest court for a better future, winning landmark cases that moved America forward," Obama said in his statement.
He successfully defended the constitutionality of the Affordable Care Act, as well as arguing in favor of gay marriage. In 2013 he led the case against the Defense of Marriage Act, a federal law that defined marriage as between a man and a woman. In 2015, he successfully argued in Obergefell v. Hodges, a decision that cleared the way for gay marriage nationwide.
This term, he defended the President's controversial executive actions on immigration as well as arguing in support of an affirmative action plan at the University of Texas.
The soft-spoken Verrilli was highly respected by the justices who sometimes offered him an opportunity -- denied to other advocates -- to take a few moments at the end of his time at the podium to sum up his argument without interruption.
In public, Verrilli spoke passionately about the pro bono work he did as a young lawyer on behalf of death row inmates.
"It was these experiences more than any other that taught me what it was to be a lawyer," he told students at Boston University School of law in 2013.
"And I also came to appreciate the importance of the principle that every person deserves vigorous advocacy " he said.
Obama nominated Verrilli to succeed Elena Kagan as solicitor general after she was sworn into the position of Associate Justice of the Supreme Court. He was confirmed by the Senate in 2011 by a 72-16 vote.
The timing of Verrilli's departure is no surprise, since Obama's second term is ending and arguments before high court have ended for this term. The court has 24 cases left to decide in its current term and is expected to complete its work by the end of June.
In a statement, Lynch called Verrilli "a brilliant lawyer, a devoted public servant and one of the most consequential solicitors general in American history."
Other analysts agreed with the historical relevance of his five years in the post.
"It's hard to imagine a solicitor general who has had a more tumultuous -- and momentous -- five years than Don Verrilli," said Steve Vladeck, CNN contributor and professor of law at American University Washington College of Law.
"Although he has received a lot of criticism for his positions and performances in some of the more high-profile cases he's argued on behalf of the Obama administration the results generally bely those criticisms, and I'm hard-pressed to think of a solicitor general who's navigated more complex waters with as much skill and grace as he has," he said.
In 2012, critics seized on Verrilli's performance at oral arguments in the health care case when he appeared to stumble after apparently choking on water at the start of his presentation.
But Verrilli was vindicated months later when Chief Justice John Roberts accepted the administration's secondary argument upholding the law under Congress' taxing power.
Prior to his government service he was a partner at Jenner & Block where he handled numerous cases before the court including MGM Studios v. Grokster, a critical copyright case concerning the unauthorized distribution of protected works.
Verrill graduated from Yale University and Columbia Law School and served as a clerk to Justice William J. Brennan Jr.