After the FBI, he served as Senior Counsel for Law Enforcement and Intelligence at the US Treasury Department and as the Assistant Inspector General for Investigations and Special Inquiries at the National Security Agency (where he was a member of the Defense Intelligence Senior Executive Service).

In 2010, he left the NSA to serve as the Deputy Inspector General at the Office of the Director of National Intelligence.

In August 2011, McCullough was nominated by President Barack Obama as the first Inspector General of the United States Intelligence Community.

McCullough's office, along with the State Department OIG, played a significant role in the initial handling of the controversy regarding Hillary Clinton's emails.

His father, Irvin Charles McCullough, Jr., was the Executive Director of the Pennsylvania Interscholastic Athletic Association, and, in the 1950s, a multi-year member of the OCBP.