diff --git a/NEWS.md b/NEWS.md
index 69719c4c4..b3a073ad6 100644
--- a/NEWS.md
+++ b/NEWS.md
@@ -23,6 +23,7 @@
 * Add a new "progress" display to the `tar_watch()` app to show verbose progress info and metadata.
 * Add a new `workspace_on_error` argument of `tar_option_set()` to supersede `error = "workspace"`. Helps control workspace behavior independently of the `error` argument of `tar_target()` (#405, #533, #534, @mattwarkentin, @xinstein).
 * Implement `error = "abridge"` in `tar_target()` and related functions. If a target errors out with this option, the target itself stops, any currently running targets keeps, and no new targets launch after that (#533, #534, @xinstein).
+* Add a menu prompt to `tar_destroy()` which can be suppressed with `TAR_ASK = "false"` (#542, @gofford).
 
 ## Deprecations
 
diff --git a/R/tar_destroy.R b/R/tar_destroy.R
index ac8cbe8ad..b648bff0f 100644
--- a/R/tar_destroy.R
+++ b/R/tar_destroy.R
@@ -23,6 +23,10 @@
 #'     automatically get deleted except if R crashed.
 #'   * `"workspaces"`: compressed files in `workspaces/` in the data store with
 #'     the saved workspaces of targets. See [tar_workspace()] for details.
+#' @param ask Logical of length 1, whether to pause with a menu prompt
+#'   before deleting files. To disable this menu, set the `TAR_ASK`
+#'   environment variable to `"false"`. `usethis::edit_r_environ()`
+#'   can help set environment variables.
 #' @examples
 #' if (identical(Sys.getenv("TAR_EXAMPLES"), "true")) {
 #' tar_dir({ # tar_dir() runs code from a temporary directory.
@@ -42,17 +46,21 @@ tar_destroy <- function(
     "scratch",
     "workspaces"
   ),
+  ask = NULL,
   store = targets::tar_config_get("store")
 ) {
-  switch(
+  path <- switch(
     match.arg(destroy),
-    all = unlink(store, recursive = TRUE),
-    meta = unlink(path_meta(store)),
-    process = unlink(path_process(store)),
-    progress = unlink(path_progress(store)),
-    objects = unlink(path_objects_dir(store), recursive = TRUE),
-    scratch = unlink(path_scratch_dir(store), recursive = TRUE),
-    workspaces = unlink(path_workspaces_dir(store), recursive = TRUE)
+    all = store,
+    meta = path_meta(store),
+    process = path_process(store),
+    progress = path_progress(store),
+    objects = path_objects_dir(store),
+    scratch = path_scratch_dir(store),
+    workspaces = path_workspaces_dir(store)
   )
+  if (tar_should_delete(path = path, ask = ask)) {
+    unlink(path, recursive = TRUE)
+  }
   invisible()
 }
diff --git a/R/tar_github_actions.R b/R/tar_github_actions.R
index 20329d04b..9273a3792 100644
--- a/R/tar_github_actions.R
+++ b/R/tar_github_actions.R
@@ -41,7 +41,7 @@ tar_github_actions <- function(
 ) {
   tar_assert_chr(path, "path must be a character")
   tar_assert_scalar(path, "path must have length 1")
-  if (!tar_should_overwrite(ask, path)) {
+  if (!tar_should_overwrite(path = path, ask = ask)) {
     # covered in tests/interactive/test-tar_github_actions.R # nolint
     return(invisible()) # nocov
   }
diff --git a/R/tar_script.R b/R/tar_script.R
index 40fbc1302..289eeb906 100644
--- a/R/tar_script.R
+++ b/R/tar_script.R
@@ -66,7 +66,7 @@ tar_script <- function(
   ask = NULL,
   script = targets::tar_config_get("script")
 ) {
-  if (!tar_should_overwrite(ask, script)) {
+  if (!tar_should_overwrite(path = script, ask = ask)) {
     # covered in tests/interactive/test-tar_script.R # nolint
     return(invisible()) # nocov
   }
diff --git a/R/utils_ask.R b/R/utils_ask.R
index 547763d22..13a7a06e5 100644
--- a/R/utils_ask.R
+++ b/R/utils_ask.R
@@ -1,8 +1,27 @@
-tar_should_overwrite <- function(ask = NULL, file = character(0)) {
+tar_should_delete <- function(path, ask) {
+  prompt <- paste0("Delete ", path, "?")
+  tar_should_modify_path(path = path, ask = ask, prompt = prompt)
+}
+
+tar_should_overwrite <- function(path, ask) {
+  prompt <- paste0("Overwrite ", path, "?")
+  tar_should_modify_path(path = path, ask = ask, prompt = prompt)
+}
+
+tar_should_modify_path <- function(
+  path = character(0),
+  ask = NULL,
+  prompt = character(0)
+) {
   ask <- ask %|||% tar_ask_env() %|||% interactive()
   tar_assert_lgl(ask)
   tar_assert_scalar(ask)
-  if (!file.exists(file) || !ask) {
+  prompt <- paste(
+    prompt,
+    "(Set the TAR_ASK environment variable to \"false\"",
+    "to disable this menu, e.g. usethis::edit_r_environ().)"
+  )
+  if (!file.exists(path) || !ask) {
     return(TRUE)
   }
   # This part is intrinsically interactive and cannot be covered
@@ -10,7 +29,7 @@ tar_should_overwrite <- function(ask = NULL, file = character(0)) {
   # tests/interactive/test-tar_script.R is an example of a semi-automated test
   # that coveres this.
   # nocov start
-  out <- utils::menu(c("yes", "no"), title = paste0("Overwrite ", file, "?"))
+  out <- utils::menu(c("yes", "no"), title = prompt)
   identical(as.integer(out), 1L)
   # nocov end
 }
diff --git a/inst/WORDLIST b/inst/WORDLIST
index 979586ecd..69f92c147 100644
--- a/inst/WORDLIST
+++ b/inst/WORDLIST
@@ -246,6 +246,7 @@ reproducibly
 rerender
 RL
 rmarkdown
+rmedicine
 Rmd
 RMSPE
 roadmap
@@ -267,6 +268,8 @@ skippable
 SLURM
 SSP
 Stallman
+Stan
+stan
 Stawitz
 storr
 Storr
diff --git a/man/tar_destroy.Rd b/man/tar_destroy.Rd
index e6d73c7a6..676924ad6 100644
--- a/man/tar_destroy.Rd
+++ b/man/tar_destroy.Rd
@@ -6,6 +6,7 @@
 \usage{
 tar_destroy(
   destroy = c("all", "meta", "process", "progress", "objects", "scratch", "workspaces"),
+  ask = NULL,
   store = targets::tar_config_get("store")
 )
 }
@@ -31,6 +32,11 @@ automatically get deleted except if R crashed.
 the saved workspaces of targets. See \code{\link[=tar_workspace]{tar_workspace()}} for details.
 }}
 
+\item{ask}{Logical of length 1, whether to pause with a menu prompt
+before deleting files. To disable this menu, set the \code{TAR_ASK}
+environment variable to \code{"false"}. \code{usethis::edit_r_environ()}
+can help set environment variables.}
+
 \item{store}{Character of length 1, path to the
 \code{targets} data store. Defaults to \code{tar_config_get("store")},
 which in turn defaults to \verb{_targets/}.
diff --git a/tests/interactive/test-tar_destroy.R b/tests/interactive/test-tar_destroy.R
new file mode 100644
index 000000000..2456f85d8
--- /dev/null
+++ b/tests/interactive/test-tar_destroy.R
@@ -0,0 +1,14 @@
+tar_test("Run tar_destroy() interactively.", {
+  tar_script()
+  tar_make()
+  old_tar_ask <- Sys.getenv("TAR_ASK")
+  Sys.setenv(TAR_ASK = "true")
+  expect_true(file.exists("_targets"))
+  tar_destroy() # See a menu and choose 2.
+  expect_true(file.exists("_targets"))
+  tar_destroy() # See a menu and choose 0.
+  expect_true(file.exists("_targets"))
+  tar_destroy() # See a menu and choose 1.
+  expect_false(file.exists("_targets"))
+  Sys.setenv(TAR_ASK = old_tar_ask)
+})
diff --git a/tests/testthat/test-utils_ask.R b/tests/testthat/test-utils_ask.R
index 415a1525c..835f9b411 100644
--- a/tests/testthat/test-utils_ask.R
+++ b/tests/testthat/test-utils_ask.R
@@ -9,9 +9,9 @@ tar_test("tar_ask_env()", {
 
 tar_test("tar_should_overwrite", {
   tmp <- tempfile()
-  expect_true(tar_should_overwrite(ask = TRUE, file = tmp))
-  expect_true(tar_should_overwrite(ask = FALSE, file = tmp))
+  expect_true(tar_should_overwrite(path = tmp, ask = TRUE))
+  expect_true(tar_should_overwrite(path = tmp, ask = FALSE))
   file.create(tmp)
-  expect_true(tar_should_overwrite(ask = FALSE, file = tmp))
+  expect_true(tar_should_overwrite(path = tmp, ask = FALSE))
   # More testing is in tests/interactive/test-tar_script.R # nolint.
 })