In 1987, Miller graduated from Columbia University, where he earned a BA in biology and psychology. He received his PhD in cognitive psychology from Stanford University in 1993 under the guidance of Roger Shepard.
Miller held positions as a postdoctoral researcher in the evolutionary and adaptive systems group in the School of Cognitive and Computing Sciences at the University of Sussex (1992–94); lecturer in the department of psychology at the University of Nottingham (1995), both in England; research scientist at the Center for Adaptive Behavior and Cognition at the Max Planck Institute for Psychological Research, Munich, Germany (1995–96); and senior research fellow at the Centre for Economic Learning and Social Evolution, University College London, England, (1996–2000). He has worked at the University of New Mexico since 2001, where he is now associate professor. In 2009, he was visiting scientist at the Genetic Epidemiology Group, Queensland Institute of Medical Research, Australia.
In 2015, in collaboration with Pickup Artist Tucker Max, Miller launched The Mating Grounds, a podcast and blog offering advice about men's sexual strategies.
The starting point for Miller's work was Charles Darwin's theoretical observation that evolution is driven not just by natural selection, but by the process called sexual selection. In support of his views on sexual selection in human evolution, he has written The Mating Mind: How Sexual Choice Shaped the Evolution of Human Nature, which states that human mate choices, courtship behavior, behavior genetics, psychometrics, and life cycle patterns support the survival value of traits related to sexual selection, such as art, morality, language, and creativity. He states that the adaptive design features of these traits suggest that they evolved through mutual mate-choice by both sexes to advertise intelligence, creativity, moral character, and heritable fitness. He also consistently cites the Fisherian runaway, a model created by Ronald Fisher to explain phenomena such as the peacock's plumage as forming through a positive feedback loop through sexual selection, as well as the handicap principle.
In an article entitled What should we be worried about? he talked about eugenics in China and how Deng Xiaoping instigated the one-child policy, "partly to curtail China's population explosion, but also to reduce dysgenic fertility". He argued that if China is successful, and given what he calls the lottery of Mendelian genetics it may increase the IQ of its population, perhaps by 5–15 IQ points per generation, concluding that within a couple of generations it "would be game over for Western global competitiveness" and hopes the West will join China in this experiment rather than citing "bioethical panic" in order to attack these policies.
In Miller's 2009 book Spent: Sex, Evolution and the Secrets of Consumerism he has used Darwinism to gain an understanding of consumerism and how marketing has exploited our inherited instincts to display social status for reproductive advantage. Miller argues that in the modern marketing-dominated culture, "coolness" at the conscious level, and the consumption choices it drives, is an aberration of the genetic legacy of two million years of living in small groups, where social status has been a critical force in reproduction. Miller's thesis is that marketing persuades people — particularly the young — that the most effective way to display that status is through consumption choices, rather than conveying such traits as intelligence and personality through more natural means of communication, such as simple conversation.
Miller argues that marketing limits its own success by using simplistic models of human nature, lacking the insights of evolutionary psychology and behavioural ecology, with a belief "that premium products are bought to display wealth, status, and taste, and they miss the deeper mental traits that people are actually wired to display, traits such as kindness, intelligence, and creativity" which limits the success of marketing.
Miller's clinical interests are the application of fitness indicator theory to understand the symptoms, demographics, and behavior genetics of schizophrenia and mood disorders. His other interests include the origins of human preferences, aesthetics, utility functions, human strategic behavior, game theory, experiment-based economics, the ovulatory effects on female mate preferences, and the intellectual legacies of Darwin, Friedrich Nietzsche, and Thorstein Veblen.
In 2007, Miller (with Joshua Tybur and Brent Jordan) published an article in Evolution and Human Behavior, concluding that lap dancers make more money during ovulation. For this paper, Miller won the 2008 Ig Nobel Award in Economics.
On June 2, 2013, Miller posted a tweet on Twitter stating: "Dear obese PhD applicants: if you didn't have the willpower to stop eating carbs, you won't have the willpower to do a dissertation #truth". Miller subsequently removed the tweet and issued two apologies, one of which said: "My sincere apoplogies to all for that idiotic, impulsive, and badly judged tweet. It does not reflect my true views, values, or standards", but not before the post was picked up by major news sources. Feminist blogs criticized the post as did Linda Bacon, a professor of nutrition at the University of California Davis. Pascal Wallisch, research scientist at the Center for Neural Science at New York University, argued that, regardless of whether or not the claim is offensive, it is factually incorrect.
Miller says that the tweet was part of a research project. The institutional review boards of University of New Mexico, Miller's home university, and New York University, where he was a visiting professor, released statements saying that Miller's tweet was "self-promotional" and cannot be considered research. The University of New Mexico formally censured Miller in August 2013.
On May 29, 2017, Miller made another controversial tweet in which he compared refugees to the Uruk-hai, a fictional race of orc warriors who invade the human kingdom of Gondor in J. R. R. Tolkien's novel, The Lord of the Rings. The Mating Mind: How Sexual Choice Shaped Human Nature (2000)
Spent: Sex, Evolution, and Consumer Behavior (2009)
With Tucker Max: Mate: Become the Man Women Want (2015)