diff --git a/NEWS.md b/NEWS.md
index 53e61e64..10ddeb9c 100644
--- a/NEWS.md
+++ b/NEWS.md
@@ -1,5 +1,8 @@
 # htmltools (development version)
 
+* `includeCSS()`, `includeHTML()`, `includeText()`, `includeMarkdown()`, and `includeScript()` now raise a clear error naming the missing file when `path` does not exist, instead of the vague "cannot open the connection" message from `readLines()`. (rstudio/shiny#1757)
+
+
 # htmltools 0.5.9
 
 * Fix test for testthat 3.3.0. (#442) 
diff --git a/R/tags.R b/R/tags.R
index f8421384..b8bb9aa6 100644
--- a/R/tags.R
+++ b/R/tags.R
@@ -1735,6 +1735,7 @@ knit_print.html_dependency <- knit_print.shiny.tag
 #' @aliases includeHTML
 #' @export
 includeHTML <- function(path) {
+  check_include_path(path, "HTML file")
   lines <- readLines(path, warn=FALSE, encoding='UTF-8')
 
   if (detect_html_document(lines)) {
@@ -1783,6 +1784,7 @@ detect_html_document <- function(lines) {
 #' @rdname include
 #' @export
 includeText <- function(path) {
+  check_include_path(path, "Text file")
   lines <- readLines(path, warn=FALSE, encoding='UTF-8')
   return(paste8(lines, collapse='\n'))
 }
@@ -1792,6 +1794,7 @@ includeText <- function(path) {
 #' @rdname include
 #' @export
 includeMarkdown <- function(path) {
+  check_include_path(path, "Markdown file")
   # markdown >= v1.3 switched from markdownToHTML() to mark()
   html <- if (packageVersion("markdown") < "1.3") {
     markdown::markdownToHTML(path, fragment.only = TRUE)
@@ -1806,6 +1809,7 @@ includeMarkdown <- function(path) {
 #' @rdname include
 #' @export
 includeCSS <- function(path, ...) {
+  check_include_path(path, "CSS file")
   lines <- readLines(path, warn=FALSE, encoding='UTF-8')
   args <- dots_list(...)
   if (is.null(args$type))
@@ -1817,10 +1821,29 @@ includeCSS <- function(path, ...) {
 #' @rdname include
 #' @export
 includeScript <- function(path, ...) {
+  check_include_path(path, "Script file")
   lines <- readLines(path, warn=FALSE, encoding='UTF-8')
   return(tags$script(HTML(paste8(lines, collapse='\n')), ...))
 }
 
+check_include_path <- function(path, what = "File", call = rlang::caller_env()) {
+  if (!rlang::is_string(path) || !nzchar(path)) {
+    rlang::abort(
+      paste0(what, " path must be a single non-empty string."),
+      call = call
+    )
+  }
+  if (!file.exists(path) || dir.exists(path)) {
+    rlang::abort(
+      c(
+        paste0(what, " does not exist."),
+        "x" = paste0("Path: ", path)
+      ),
+      call = call
+    )
+  }
+}
+
 #' Include content only once
 #'
 #' Use `singleton` to wrap contents (tag, text, HTML, or lists) that should
diff --git a/tests/testthat/test-tags.r b/tests/testthat/test-tags.r
index 195c1f86..4fd3f8bf 100644
--- a/tests/testthat/test-tags.r
+++ b/tests/testthat/test-tags.r
@@ -1226,3 +1226,39 @@ test_that("includeHTML() warns if full document is detected", {
   save_html(p("test"), tmp_html)
   expect_warning(includeHTML(tmp_html))
 })
+
+test_that("include*() helpers raise a clear error when the file is missing", {
+  missing <- tempfile("does-not-exist-", fileext = ".txt")
+  expect_false(file.exists(missing))
+
+  expect_error(includeCSS(missing),    "CSS file does not exist")
+  expect_error(includeHTML(missing),   "HTML file does not exist")
+  expect_error(includeText(missing),   "Text file does not exist")
+  expect_error(includeScript(missing), "Script file does not exist")
+})
+
+test_that("includeMarkdown() raises a clear error when the file is missing", {
+  skip_if_not_installed("markdown")
+  missing <- tempfile("does-not-exist-", fileext = ".txt")
+  expect_error(includeMarkdown(missing), "Markdown file does not exist")
+})
+
+test_that("include*() missing-file error is attributed to the public helper", {
+  missing <- tempfile("does-not-exist-", fileext = ".txt")
+  err <- rlang::catch_cnd(includeCSS(missing))
+  expect_match(rlang::expr_deparse(err$call), "includeCSS")
+})
+
+test_that("include*() helpers reject invalid path inputs", {
+  expect_error(includeCSS(NULL),         "must be a single non-empty string")
+  expect_error(includeCSS(character(0)), "must be a single non-empty string")
+  expect_error(includeCSS(c("a", "b")),  "must be a single non-empty string")
+  expect_error(includeCSS(""),           "must be a single non-empty string")
+  expect_error(includeCSS(NA_character_), "must be a single non-empty string")
+})
+
+test_that("include*() helpers reject a directory path", {
+  dir <- withr::local_tempdir()
+  expect_true(dir.exists(dir))
+  expect_error(includeCSS(dir), "CSS file does not exist")
+})