diff --git a/NEWS.md b/NEWS.md
index 407d8316..d34af1a7 100644
--- a/NEWS.md
+++ b/NEWS.md
@@ -4,6 +4,7 @@
 
 * Added support for graphic devices provided by ragg and svglite (@thomasp85 #964)
 * `parse_rds()`, `parse_feather()`, and `parse_parquet()` no longer writes data to disk during parsing (@thomasp85, #942)
+* Returning error messages are now turned off by default rather than being turned on if running interactively and turned off if not (@thomasp85, #962)
 
 # plumber 1.2.2
 
diff --git a/R/plumber.R b/R/plumber.R
index 0cad0ec6..eed20aef 100644
--- a/R/plumber.R
+++ b/R/plumber.R
@@ -143,7 +143,7 @@ Plumber <- R6Class(
     #' Mac OS X, port numbers smaller than 1025 require root privileges.
     #'
     #' This value does not need to be explicitly assigned. To explicitly set it, see [options_plumber()].
-    #' @param debug If `TRUE`, it will provide more insight into your API errors. Using this value will only last for the duration of the run. If a `$setDebug()` has not been called, `debug` will default to `interactive()` at `$run()` time. See `$setDebug()` for more details.
+    #' @param debug If `TRUE`, it will provide more insight into your API errors. Using this value will only last for the duration of the run. If a `$setDebug()` has not been called, `debug` will default to `FALSE` at `$run()` time. See `$setDebug()` for more details.
     #' @param swagger Deprecated. Please use `docs` instead. See `$setDocs(docs)` or `$setApiSpec()` for more customization.
     #' @param swaggerCallback An optional single-argument function that is
     #'   called back with the URL to an OpenAPI user interface when one becomes
@@ -223,17 +223,16 @@ Plumber <- R6Class(
           )
         )
 
-      # Delay the setting of debug as long as possible.
-      # The router could be made in an interactive setting and used in background process.
-      # Do not determine if interactive until run time
+      # Temporarily set the debug value
       prev_debug <- private$debug
       on.exit({
         private$debug <- prev_debug
       }, add = TRUE)
-      # Fix the debug value while running.
+      # Determine if the user should be informed about default behavior
+      inform_debug <- is.null(prev_debug) && rlang::is_missing(debug)
+
+      # Set debug value, defaulting to already set value (which returns FALSE if not set)
       self$setDebug(
-        # Order: Run method param, internally set value, is interactive()
-        # `$getDebug()` is dynamic given `setDebug()` has never been called.
         rlang::maybe_missing(debug, self$getDebug())
       )
 
@@ -267,6 +266,14 @@ Plumber <- R6Class(
         on.exit(unmount_docs(self, docs_info), add = TRUE)
       }
 
+      if (!isTRUE(quiet) && inform_debug && rlang::is_interactive()) {
+        rlang::inform(
+          "Error reporting has been turned off by default. See `pr_set_debug()` for more details.\nTo disable this message, set a debug value.",
+          .frequency="once",
+          .frequency_id="pr_set_debug_message"
+        )
+      }
+
       on.exit(private$runHooks("exit"), add = TRUE)
 
       httpuv::runServer(host, port, self)
@@ -963,15 +970,15 @@ Plumber <- R6Class(
     #'
     #' See also: `$getDebug()` and [pr_set_debug()]
     #' @param debug `TRUE` provides more insight into your API errors.
-    setDebug = function(debug = interactive()) {
+    setDebug = function(debug = FALSE) {
       stopifnot(length(debug) == 1)
       private$debug <- isTRUE(debug)
     },
-    #' @description Retrieve the `debug` value. If it has never been set, the result of `interactive()` will be used.
+    #' @description Retrieve the `debug` value. If it has never been set, it will return `FALSE`.
     #'
     #' See also: `$getDebug()` and [pr_set_debug()]
     getDebug = function() {
-      private$debug %||% default_debug()
+      private$debug %||% FALSE
     },
     #' @description Add a filter to plumber router
     #'
@@ -1333,13 +1340,6 @@ upgrade_docs_parameter <- function(docs, ...) {
   )
 }
 
-
-
-default_debug <- function() {
-  interactive()
-}
-
-
 urlHost <- function(scheme = "http", host, port, path = "", changeHostLocation = FALSE) {
   if (isTRUE(changeHostLocation)) {
     # upgrade callback location to be localhost and not catch-all addresses
diff --git a/R/pr_set.R b/R/pr_set.R
index a62c8158..24fc5004 100644
--- a/R/pr_set.R
+++ b/R/pr_set.R
@@ -97,8 +97,8 @@ pr_set_error <- function(pr, fun) {
 
 #' Set debug value to include error messages of routes cause an error
 #'
-#' To hide any error messages in production, set the debug value to `FALSE`.
-#' The `debug` value is enabled by default for [interactive()] sessions.
+#' By default, error messages from your plumber routes are hidden, but can be
+#' turned on by setting the debug value to `TRUE` using this setter.
 #'
 #' @template param_pr
 #' @param debug `TRUE` provides more insight into your API errors.
@@ -118,7 +118,15 @@ pr_set_error <- function(pr, fun) {
 #'   pr_get("/boom", function() stop("boom")) %>%
 #'   pr_run()
 #' }
-pr_set_debug <- function(pr, debug = interactive()) {
+#'
+#' # Setting within a plumber file
+#' #* @plumber
+#' function(pr) {
+#'   pr %>%
+#'     pr_set_debug(TRUE)
+#' }
+#'
+pr_set_debug <- function(pr, debug = FALSE) {
   validate_pr(pr)
   pr$setDebug(debug = debug)
   pr
diff --git a/man/Plumber.Rd b/man/Plumber.Rd
index 5090da29..fea92e6d 100644
--- a/man/Plumber.Rd
+++ b/man/Plumber.Rd
@@ -242,7 +242,7 @@ This value does not need to be explicitly assigned. To explicitly set it, see \c
 
 \item{\code{swagger}}{Deprecated. Please use \code{docs} instead. See \verb{$setDocs(docs)} or \verb{$setApiSpec()} for more customization.}
 
-\item{\code{debug}}{If \code{TRUE}, it will provide more insight into your API errors. Using this value will only last for the duration of the run. If a \verb{$setDebug()} has not been called, \code{debug} will default to \code{interactive()} at \verb{$run()} time. See \verb{$setDebug()} for more details.}
+\item{\code{debug}}{If \code{TRUE}, it will provide more insight into your API errors. Using this value will only last for the duration of the run. If a \verb{$setDebug()} has not been called, \code{debug} will default to \code{FALSE} at \verb{$run()} time. See \verb{$setDebug()} for more details.}
 
 \item{\code{swaggerCallback}}{An optional single-argument function that is
 called back with the URL to an OpenAPI user interface when one becomes
@@ -788,7 +788,7 @@ Set debug value to include error messages.
 
 See also: \verb{$getDebug()} and \code{\link[=pr_set_debug]{pr_set_debug()}}
 \subsection{Usage}{
-\if{html}{\out{<div class="r">}}\preformatted{Plumber$setDebug(debug = interactive())}\if{html}{\out{</div>}}
+\if{html}{\out{<div class="r">}}\preformatted{Plumber$setDebug(debug = FALSE)}\if{html}{\out{</div>}}
 }
 
 \subsection{Arguments}{
@@ -803,7 +803,7 @@ See also: \verb{$getDebug()} and \code{\link[=pr_set_debug]{pr_set_debug()}}
 \if{html}{\out{<a id="method-Plumber-getDebug"></a>}}
 \if{latex}{\out{\hypertarget{method-Plumber-getDebug}{}}}
 \subsection{Method \code{getDebug()}}{
-Retrieve the \code{debug} value. If it has never been set, the result of \code{interactive()} will be used.
+Retrieve the \code{debug} value. If it has never been set, it will return \code{FALSE}.
 
 See also: \verb{$getDebug()} and \code{\link[=pr_set_debug]{pr_set_debug()}}
 \subsection{Usage}{
diff --git a/man/pr_set_debug.Rd b/man/pr_set_debug.Rd
index cfeb9b3d..66d73da2 100644
--- a/man/pr_set_debug.Rd
+++ b/man/pr_set_debug.Rd
@@ -4,7 +4,7 @@
 \alias{pr_set_debug}
 \title{Set debug value to include error messages of routes cause an error}
 \usage{
-pr_set_debug(pr, debug = interactive())
+pr_set_debug(pr, debug = FALSE)
 }
 \arguments{
 \item{pr}{A Plumber API. Note: The supplied Plumber API object will also be updated in place as well as returned by the function.}
@@ -15,8 +15,8 @@ pr_set_debug(pr, debug = interactive())
 The Plumber router with the new debug setting.
 }
 \description{
-To hide any error messages in production, set the debug value to \code{FALSE}.
-The \code{debug} value is enabled by default for \code{\link[=interactive]{interactive()}} sessions.
+By default, error messages from your plumber routes are hidden, but can be
+turned on by setting the debug value to \code{TRUE} using this setter.
 }
 \examples{
 \dontrun{
@@ -32,4 +32,12 @@ pr() \%>\%
   pr_get("/boom", function() stop("boom")) \%>\%
   pr_run()
 }
+
+# Setting within a plumber file
+#* @plumber
+function(pr) {
+  pr \%>\%
+    pr_set_debug(TRUE)
+}
+
 }
diff --git a/tests/testthat/test-plumber-run.R b/tests/testthat/test-plumber-run.R
index fe20210a..12d1eeb8 100644
--- a/tests/testthat/test-plumber-run.R
+++ b/tests/testthat/test-plumber-run.R
@@ -93,41 +93,3 @@ test_that("`swaggerCallback` can be set by option after the pr is created", {
   mockery::expect_called(m, 1)
 
 })
-
-
-### Test does not work as expected with R6 objects.
-test_that("`debug` is not set until runtime", {
-  skip_if_not_installed("mockery", "0.4.2")
-
-  m <- mockery::mock(TRUE, cycle = TRUE)
-  local_mocked_bindings(default_debug = m)
-
-  root <- pr()
-  root$getDebug()
-  mockery::expect_called(m, 1)
-
-  with_interrupt({
-    root %>% pr_run(quiet = TRUE)
-  })
-  # increase by 1
-  mockery::expect_called(m, 2)
-
-  # listen to set value
-  with_interrupt({
-    root %>%
-      pr_set_debug(TRUE) %>%
-      pr_run(quiet = TRUE)
-  })
-  # not updated. stay at 2
-  mockery::expect_called(m, 2)
-
-  # listen to run value
-  with_interrupt({
-    root %>%
-      pr_run(debug = FALSE, quiet = TRUE)
-  })
-  # not updated. stay at 2
-  mockery::expect_called(m, 2)
-
-  # TODO test that run(debug=) has preference over pr_set_debug()
-})