diff --git a/.lintr b/.lintr
index fbe54d2ce..8420e7ba5 100644
--- a/.lintr
+++ b/.lintr
@@ -1,5 +1,5 @@
 linters: all_linters(
-    backport_linter("3.6.0", except = c("R_user_dir", "deparse1", "...names")),
+    backport_linter("auto", except = c("R_user_dir", "deparse1", "...names")),
     line_length_linter(120L),
     object_overwrite_linter(allow_names = c("line", "lines", "pipe", "symbols")),
     todo_comment_linter(
diff --git a/R/backport_linter.R b/R/backport_linter.R
index 546463072..b652b4a45 100644
--- a/R/backport_linter.R
+++ b/R/backport_linter.R
@@ -2,9 +2,11 @@
 #'
 #' Check for usage of unavailable functions. Not reliable for testing r-devel dependencies.
 #'
-#' @param r_version Minimum R version to test for compatibility. Defaults to
-#'  the R version currently in use. The version can be specified as a version
-#'  number, or as a version alias (such as `"devel"`, `"oldrel"`, `"oldrel-1"`).
+#' @param r_version Minimum R version to test for compatibility. The version
+#'  can be specified as a version number, or as a version alias (such as `"devel"`,
+#'  `"oldrel"`, `"oldrel-1"`). It can also be `"auto"` (the default) to use the minimum R version 
+#'   declared in the `DESCRIPTION` file of R packages, and the R version in the current
+#'   R session outside of packages.
 #' @param except Character vector of functions to be excluded from linting.
 #'  Use this to list explicitly defined backports, e.g. those imported from the `{backports}` package or manually
 #'  defined in your package.
@@ -46,7 +48,7 @@
 #' @evalRd rd_tags("backport_linter")
 #' @seealso [linters] for a complete list of linters available in lintr.
 #' @export
-backport_linter <- function(r_version = getRversion(), except = character()) {
+backport_linter <- function(r_version = "auto", except = character()) {
   r_version <- normalize_r_version(r_version)
 
   if (all(r_version >= R_system_version(names(backports)))) {
@@ -120,6 +122,15 @@ normalize_r_version <- function(r_version) {
     ))
 
     r_version <- R_system_version(available_patches[selected_patch])
+  } else if (identical(r_version, "auto")) {
+    r_version <- min_r_version()
+    if (is.na(r_version)) {
+      cli_warn(c(
+        x = "No DESCRIPTION file or no specified minimum R version could be found.",
+        i = "Setting {.arg r_version} to the currently running R version (R {getRversion()})."
+      ))
+      r_version <- getRversion()
+    }
   } else if (is.character(r_version)) {
     r_version <- R_system_version(r_version, strict = TRUE)
   } else if (!inherits(r_version, "R_system_version")) {
diff --git a/R/settings_utils.R b/R/settings_utils.R
index 166dd362a..7a9be2784 100644
--- a/R/settings_utils.R
+++ b/R/settings_utils.R
@@ -112,3 +112,23 @@ pkg_name <- function(path = find_package()) {
   nm <- read.dcf(file.path(path, "DESCRIPTION"), fields = "Package")[1L]
   if (!is.na(nm)) nm
 }
+
+min_r_version <- function(path = find_package(".")) {
+  if (is.null(path)) {
+    return(NA_character_)
+  }
+  depends_field <- read.dcf(file.path(path, "DESCRIPTION"), fields = "Depends")
+
+  depends <- trimws(strsplit(depends_field, ",", fixed = TRUE)[[1L]])
+
+  min_r_ver <- gsub("^R \\(>=?\\s(.+)\\)", "\\1", grep("R ", depends, value = TRUE, fixed = TRUE))
+
+  if (length(min_r_ver) == 0L) {
+    return(NA_character_)
+  }
+  # According to 'Writing R Extensions', the trailing 0 for patch version can
+  # be dropped.
+  # But we want to identically match an existing version number so we add it if
+  # it's missing.
+  gsub("^(\\d+\\.\\d+)$", "\\1.0", min_r_ver)
+}
diff --git a/man/backport_linter.Rd b/man/backport_linter.Rd
index 22c97ebbe..09616adb3 100644
--- a/man/backport_linter.Rd
+++ b/man/backport_linter.Rd
@@ -4,12 +4,14 @@
 \alias{backport_linter}
 \title{Backport linter}
 \usage{
-backport_linter(r_version = getRversion(), except = character())
+backport_linter(r_version = "auto", except = character())
 }
 \arguments{
-\item{r_version}{Minimum R version to test for compatibility. Defaults to
-the R version currently in use. The version can be specified as a version
-number, or as a version alias (such as \code{"devel"}, \code{"oldrel"}, \code{"oldrel-1"}).}
+\item{r_version}{Minimum R version to test for compatibility. The version
+can be specified as a version number, or as a version alias (such as \code{"devel"},
+\code{"oldrel"}, \code{"oldrel-1"}). It can also be \code{"auto"} (the default) to use the minimum R version
+declared in the \code{DESCRIPTION} file of R packages, and the R version in the current
+R session outside of packages.}
 
 \item{except}{Character vector of functions to be excluded from linting.
 Use this to list explicitly defined backports, e.g. those imported from the \code{{backports}} package or manually
diff --git a/tests/testthat/dummy_packages/auto_backport_fail/DESCRIPTION b/tests/testthat/dummy_packages/auto_backport_fail/DESCRIPTION
new file mode 100644
index 000000000..bccb4eb31
--- /dev/null
+++ b/tests/testthat/dummy_packages/auto_backport_fail/DESCRIPTION
@@ -0,0 +1,3 @@
+Package: mypkg
+Version: 0.1.0
+Depends: R (>= 4.0.0)
\ No newline at end of file
diff --git a/tests/testthat/dummy_packages/auto_backport_fail/R/my_numtobits.R b/tests/testthat/dummy_packages/auto_backport_fail/R/my_numtobits.R
new file mode 100644
index 000000000..4ccb43c0b
--- /dev/null
+++ b/tests/testthat/dummy_packages/auto_backport_fail/R/my_numtobits.R
@@ -0,0 +1,3 @@
+my_numtobits <- function() {
+  numToBits(2)
+}
diff --git a/tests/testthat/dummy_packages/auto_backport_pass/DESCRIPTION b/tests/testthat/dummy_packages/auto_backport_pass/DESCRIPTION
new file mode 100644
index 000000000..487b50b48
--- /dev/null
+++ b/tests/testthat/dummy_packages/auto_backport_pass/DESCRIPTION
@@ -0,0 +1,3 @@
+Package: mypkg
+Version: 0.1.0
+Depends: R (>= 4.2.0)
\ No newline at end of file
diff --git a/tests/testthat/dummy_packages/auto_backport_pass/R/my_numtobits.R b/tests/testthat/dummy_packages/auto_backport_pass/R/my_numtobits.R
new file mode 100644
index 000000000..4ccb43c0b
--- /dev/null
+++ b/tests/testthat/dummy_packages/auto_backport_pass/R/my_numtobits.R
@@ -0,0 +1,3 @@
+my_numtobits <- function() {
+  numToBits(2)
+}
diff --git a/tests/testthat/test-backport_linter.R b/tests/testthat/test-backport_linter.R
index 9b2d47bfe..b20305627 100644
--- a/tests/testthat/test-backport_linter.R
+++ b/tests/testthat/test-backport_linter.R
@@ -10,7 +10,8 @@ test_that("backport_linter detects backwards-incompatibility", {
   expect_no_lint(".getNamespaceInfo(dir.exists(lapply(x, toTitleCase)))", backport_linter())
   expect_no_lint(".getNamespaceInfo(dir.exists(lapply(x, toTitleCase)))", backport_linter("release"))
   expect_no_lint(".getNamespaceInfo(dir.exists(lapply(x, toTitleCase)))", backport_linter("devel"))
-
+  expect_no_lint(".getNamespaceInfo(dir.exists(lapply(x, toTitleCase)))", backport_linter("auto"))
+  
   expect_lint(
     "numToBits(2)",
     rex::rex("numToBits (R 4.1.0) is not always available for requested dependency (R >= 4.0.0)."),
@@ -82,3 +83,46 @@ test_that("backport_linter generates expected warnings", {
   )
   expect_identical(l, lint(tmp, backport_linter("3.0.0")))
 })
+
+test_that("backport_linter works with package R version", {
+  pkg_lints_from_outside <- lint_package(
+    "dummy_packages/auto_backport_fail",
+    linters = backport_linter(),
+    parse_settings = FALSE
+  )
+  pkg_lints_from_root <- withr::with_dir(
+    "dummy_packages/auto_backport_fail",
+    lint_package(linters = backport_linter(), parse_settings = FALSE)
+  )
+
+  expect_length(pkg_lints_from_outside, 1L)
+  expect_identical(
+    pkg_lints_from_outside[[1]]$message,
+    "numToBits (R 4.1.0) is not always available for requested dependency (R >= 4.0.0)."
+  )
+  expect_length(pkg_lints_from_root, 1L)
+  expect_identical(
+    pkg_lints_from_root[[1]]$message,
+    "numToBits (R 4.1.0) is not always available for requested dependency (R >= 4.0.0)."
+  )
+
+  # Can be overwritten
+  pkg_lints_from_outside_noauto <- lint_package(
+    "dummy_packages/auto_backport_fail",    
+    backport_linter("3.0.0"),
+    parse_settings = FALSE
+  )
+
+  expect_length(pkg_lints_from_outside_noauto, 1L)
+  expect_identical(
+    pkg_lints_from_outside_noauto[[1]]$message,
+    "numToBits (R 4.1.0) is not always available for requested dependency (R >= 3.0.0)."
+  )
+
+  pkg_lints_auto_pass <- lint_package(
+    "dummy_packages/auto_backport_pass",
+    linters = backport_linter(),
+    parse_settings = FALSE
+  )
+  expect_length(pkg_lints_auto_pass, 0L)
+})