diff --git a/DESCRIPTION b/DESCRIPTION
index 38ade75f1..b43ec4d4c 100644
--- a/DESCRIPTION
+++ b/DESCRIPTION
@@ -50,7 +50,7 @@ Suggests:
     httr2 (>= 1.0.0),
     knitr (>= 1.39),
     lintr (>= 3.0.0),
-    quarto,
+    quarto (>= 1.5.1),
     remotes (>= 2.5.0),
     rmarkdown (>= 2.14),
     rstudioapi (>= 0.13),
diff --git a/NEWS.md b/NEWS.md
index 7c85702e2..b9e6afa76 100644
--- a/NEWS.md
+++ b/NEWS.md
@@ -13,6 +13,7 @@ Deprecations
 
 Other improvements
 
+* `build_readme()` gains support for `README.qmd` and renders using Quarto (#2620).
 * `install()` now installs dependencies with `pak::local_install_deps()` instead of `remotes::install_deps()`. This lets us default to `upgrade = FALSE`, so that existing dependencies are only upgraded when a newer version is actually required (#2486). `keep_source` now defaults to `TRUE` when `build = FALSE`, so that source references are automatically preserved during development installs.
 * `build_manual()` reports more details on failure (#2586).
 * `build_site()` now just calls `pkgdown::build_site()`, meaning that you will get more (informative) output by default (#2578).
@@ -28,8 +29,7 @@ Other improvements
 
 # devtools 2.4.6
 
-* Functions that use httr now explicitly check that it is installed
-  (@catalamarti, #2573).
+* Functions that use httr now explicitly check that it is installed (@catalamarti, #2573).
 
 * `test_coverage()` now works if the package has not been installed.
 
diff --git a/R/build-readme.R b/R/build-readme.R
index 2a7d4f94b..0e2351b17 100644
--- a/R/build-readme.R
+++ b/R/build-readme.R
@@ -4,7 +4,7 @@
 #' `r lifecycle::badge("deprecated")`
 #'
 #' `build_rmd()` is deprecated, as it is a low-level helper for internal use. To
-#' render your package's `README.Rmd` or `README.qmd`, use [build_readme()]. To
+#' render your package's `README.qmd` or `README.Rmd`, use [build_readme()]. To
 #' preview a vignette or article, use functions like [pkgdown::build_site()] or
 #' [pkgdown::build_article()].
 #'
@@ -64,9 +64,6 @@ build_rmd_impl <- function(
   output_options$html_preview <- FALSE
 
   for (path in paths) {
-    if (!quiet) {
-      cli::cli_inform(c(i = "Building {.path {path}}"))
-    }
     callr::r_safe(
       function(...) rmarkdown::render(...),
       args = list(
@@ -86,36 +83,77 @@ build_rmd_impl <- function(
 
 #' Build README
 #'
-#' Renders an executable README, such as `README.Rmd`, to `README.md`.
-#' Specifically, `build_readme()`:
+#' Renders an executable README, i.e. `README.qmd` or `README.Rmd`, to
+#' `README.md`. Specifically, `build_readme()`:
 #' * Installs a copy of the package's current source to a temporary library
 #' * Renders the README in a clean R session
 #'
-#' @param path Path to the package to build the README.
+#' @param path Path to the top-level directory of the source package.
 #' @param quiet If `TRUE`, suppresses most output. Set to `FALSE`
 #'   if you need to debug.
-#' @param ... Additional arguments passed to [rmarkdown::render()].
+#' @param ... Additional arguments passed to [rmarkdown::render()], in the
+#'   case of `README.Rmd`. Not used for `README.qmd`
 #' @export
 build_readme <- function(path = ".", quiet = TRUE, ...) {
   pkg <- as.package(path)
 
-  regexp <- paste0(path_file(pkg$path), "/(inst/)?readme[.]rmd$")
-  readme_path <- path_abs(dir_ls(
-    pkg$path,
-    ignore.case = TRUE,
-    regexp = regexp,
-    recurse = 1,
-    type = "file"
-  ))
+  readme_candidates <- c(
+    path(pkg$path, "README.qmd"),
+    path(pkg$path, "README.Rmd"),
+    path(pkg$path, "inst", "README.qmd"),
+    path(pkg$path, "inst", "README.Rmd")
+  )
+  readme_path <- readme_candidates[file_exists(readme_candidates)]
 
   if (length(readme_path) == 0) {
-    cli::cli_abort("Can't find {.file README.Rmd} or {.file inst/README.Rmd}.")
+    cli::cli_abort(
+      "Can't find {.file README.qmd} or {.file README.Rmd}, at the top-level or
+      below {.file inst/}."
+    )
   }
   if (length(readme_path) > 1) {
+    rel_paths <- path_rel(readme_path, pkg$path)
     cli::cli_abort(
-      "Can't have both {.file README.Rmd} and {.file inst/README.Rmd}."
+      "Found multiple executable READMEs: {.file {rel_paths}}. There can only be
+      one."
     )
   }
 
-  build_rmd_impl(readme_path, path = path, quiet = quiet, ...)
+  if (!quiet) {
+    cli::cli_inform(c(i = "Building {.path {readme_path}}"))
+  }
+
+  if (path_ext(readme_path) == "qmd") {
+    build_qmd_readme(readme_path, path = path, quiet = quiet)
+  } else {
+    build_rmd_impl(readme_path, path = path, quiet = quiet, ...)
+  }
+}
+
+build_qmd_readme <- function(readme_path, path = ".", quiet = TRUE) {
+  pkg <- as.package(path)
+
+  check_installed("quarto")
+  save_all()
+
+  local_install(pkg, quiet = TRUE)
+
+  # Quarto spawns its own R process for knitr, which won't inherit .libPaths().
+
+  # Pass library paths via R_LIBS_USER so the quarto subprocess finds the
+  # temporarily installed package first, ahead of any user-installed version.
+  lib_paths <- paste(.libPaths(), collapse = .Platform$path.sep)
+
+  callr::r_safe(
+    function(input, quiet) {
+      quarto::quarto_render(input = input, quiet = quiet)
+    },
+    args = list(input = readme_path, quiet = quiet),
+    env = c(callr::rcmd_safe_env(), R_LIBS_USER = lib_paths),
+    show = TRUE,
+    spinner = FALSE,
+    stderr = "2>&1"
+  )
+
+  invisible(TRUE)
 }
diff --git a/man/build_readme.Rd b/man/build_readme.Rd
index 048f97e5c..ffcc4c76a 100644
--- a/man/build_readme.Rd
+++ b/man/build_readme.Rd
@@ -7,16 +7,17 @@
 build_readme(path = ".", quiet = TRUE, ...)
 }
 \arguments{
-\item{path}{Path to the package to build the README.}
+\item{path}{Path to the top-level directory of the source package.}
 
 \item{quiet}{If \code{TRUE}, suppresses most output. Set to \code{FALSE}
 if you need to debug.}
 
-\item{...}{Additional arguments passed to \code{\link[rmarkdown:render]{rmarkdown::render()}}.}
+\item{...}{Additional arguments passed to \code{\link[rmarkdown:render]{rmarkdown::render()}}, in the
+case of \code{README.Rmd}. Not used for \code{README.qmd}}
 }
 \description{
-Renders an executable README, such as \code{README.Rmd}, to \code{README.md}.
-Specifically, \code{build_readme()}:
+Renders an executable README, i.e. \code{README.qmd} or \code{README.Rmd}, to
+\code{README.md}. Specifically, \code{build_readme()}:
 \itemize{
 \item Installs a copy of the package's current source to a temporary library
 \item Renders the README in a clean R session
diff --git a/man/build_rmd.Rd b/man/build_rmd.Rd
index f3266f0ba..c55571d08 100644
--- a/man/build_rmd.Rd
+++ b/man/build_rmd.Rd
@@ -25,7 +25,7 @@ format is read from metadata (i.e. not a custom format object passed to
 \ifelse{html}{\href{https://lifecycle.r-lib.org/articles/stages.html#deprecated}{\figure{lifecycle-deprecated.svg}{options: alt='[Deprecated]'}}}{\strong{[Deprecated]}}
 
 \code{build_rmd()} is deprecated, as it is a low-level helper for internal use. To
-render your package's \code{README.Rmd} or \code{README.qmd}, use \code{\link[=build_readme]{build_readme()}}. To
+render your package's \code{README.qmd} or \code{README.Rmd}, use \code{\link[=build_readme]{build_readme()}}. To
 preview a vignette or article, use functions like \code{\link[pkgdown:build_site]{pkgdown::build_site()}} or
 \code{\link[pkgdown:build_articles]{pkgdown::build_article()}}.
 }
diff --git a/tests/testthat/_snaps/build-readme.md b/tests/testthat/_snaps/build-readme.md
index 841d36431..e37ab3754 100644
--- a/tests/testthat/_snaps/build-readme.md
+++ b/tests/testthat/_snaps/build-readme.md
@@ -4,7 +4,7 @@
       build_readme(pkg)
     Condition
       Error in `build_readme()`:
-      ! Can't find 'README.Rmd' or 'inst/README.Rmd'.
+      ! Can't find 'README.qmd' or 'README.Rmd', at the top-level or below 'inst/'.
 
 ---
 
@@ -12,7 +12,15 @@
       build_readme(pkg)
     Condition
       Error in `build_readme()`:
-      ! Can't have both 'README.Rmd' and 'inst/README.Rmd'.
+      ! Found multiple executable READMEs: 'README.Rmd' and 'inst/README.Rmd'. There can only be one.
+
+# errors if both README.qmd and README.Rmd exist
+
+    Code
+      build_readme(pkg)
+    Condition
+      Error in `build_readme()`:
+      ! Found multiple executable READMEs: 'README.qmd' and 'README.Rmd'. There can only be one.
 
 # build_rmd() is deprecated
 
diff --git a/tests/testthat/test-build-readme.R b/tests/testthat/test-build-readme.R
index 8afb381a0..34c1ad7ac 100644
--- a/tests/testthat/test-build-readme.R
+++ b/tests/testthat/test-build-readme.R
@@ -1,4 +1,4 @@
-test_that("can build README in root directory", {
+test_that("can build README.Rmd in root directory", {
   skip_on_cran()
 
   pkg <- local_package_create()
@@ -14,7 +14,7 @@ test_that("can build README in root directory", {
   expect_false(file_exists(path(pkg, "README.html")))
 })
 
-test_that("can build README in inst/", {
+test_that("can build README.Rmd in inst/", {
   skip_on_cran()
 
   pkg <- local_package_create()
@@ -37,6 +37,59 @@ test_that("can build README in inst/", {
   expect_false(file_exists(path(pkg, "inst", "README.html")))
 })
 
+test_that("can build README.qmd in root directory", {
+  skip_on_cran()
+  skip_if_not_installed("quarto")
+  skip_if_not(quarto::quarto_available(), "quarto cli not available")
+
+  pkg <- local_package_create()
+  # TODO: use usethis::use_readme_qmd() once it's in a usethis release
+  # https://github.com/r-lib/usethis/pull/2219
+  writeLines(
+    c(
+      "---",
+      "format: gfm",
+      "---",
+      "",
+      "# testpkg",
+      "",
+      "This is a test package."
+    ),
+    path(pkg, "README.qmd")
+  )
+
+  build_readme(pkg, quiet = TRUE)
+  expect_true(file_exists(path(pkg, "README.md")))
+})
+
+test_that("can build README.qmd in inst/", {
+  skip_on_cran()
+  skip_if_not_installed("quarto")
+  skip_if_not(quarto::quarto_available(), "quarto cli not available")
+
+  pkg <- local_package_create()
+  # TODO: use usethis::use_readme_qmd() once it's in a usethis release
+  # https://github.com/r-lib/usethis/pull/2219
+  dir_create(pkg, "inst")
+  writeLines(
+    c(
+      "---",
+      "format: gfm",
+      "---",
+      "",
+      "# testpkg",
+      "",
+      "This is a test package."
+    ),
+    path(pkg, "inst", "README.qmd")
+  )
+
+  build_readme(pkg, quiet = TRUE)
+  expect_true(file_exists(path(pkg, "inst", "README.md")))
+  expect_false(file_exists(path(pkg, "README.qmd")))
+  expect_false(file_exists(path(pkg, "README.md")))
+})
+
 test_that("useful errors if too few or too many", {
   pkg <- local_package_create()
   expect_snapshot(build_readme(pkg), error = TRUE)
@@ -52,6 +105,13 @@ test_that("useful errors if too few or too many", {
   expect_snapshot(build_readme(pkg), error = TRUE)
 })
 
+test_that("errors if both README.qmd and README.Rmd exist", {
+  pkg <- local_package_create()
+  file_create(path(pkg, "README.Rmd"))
+  file_create(path(pkg, "README.qmd"))
+  expect_snapshot(build_readme(pkg), error = TRUE)
+})
+
 test_that("don't error for README in another directory", {
   skip_on_cran()