Pistole is the third person the Obama administration has named for the position. The FBI veteran would inherit an agency that has been without a permanent leader for more than one year.
"The talent and knowledge John has acquired in more than two decades of service with the FBI will make him a valuable asset to our administration's efforts to strengthen the security and screening measures at our airports," the president said in a statement. "I am grateful that he has agreed to take on this important role, and I look forward to working with him in the weeks and months ahead."
Pistole, who began his FBI career as a special agent in 1983, led investigative and recovery efforts for the 1999 Egypt Air Flight 990 crash off the coast of Rhode Island and led an Information Security Working Group in 2001 after the espionage arrest of Robert Hanssen.
Obama's first choice for the spot, Erroll Southers, withdrew his nomination in January after Republicans jumped on news reports that indicated he had provided Congress with misleading information on whether he had accessed a federal database to obtain confidential records. GOP opponents also were concerned Southers would support efforts to grant airport screeners collective bargaining rights.
The second choice, retired Army Maj. Gen. Robert Harding, withdrew his name from consideration in March, after congressional staff learned his previous defense contracting firm was found to have overbilled the government for interrogation work in Iraq.