diff --git a/NAMESPACE b/NAMESPACE
index 561a63bc..90b86d4e 100644
--- a/NAMESPACE
+++ b/NAMESPACE
@@ -69,6 +69,7 @@ S3method(merge,rd_section_inherit_section)
 S3method(merge,rd_section_minidesc)
 S3method(merge,rd_section_param)
 S3method(merge,rd_section_prop)
+S3method(merge,rd_section_r6_class)
 S3method(merge,rd_section_reexport)
 S3method(merge,rd_section_section)
 S3method(merge,rd_section_seealso)
diff --git a/NEWS.md b/NEWS.md
index 01257b6a..70a4d99b 100644
--- a/NEWS.md
+++ b/NEWS.md
@@ -74,7 +74,7 @@ See `vignette("rd-S7")` for best practices.
 
 ## Individual tags
 
-* Tags that expect single-line input now warn when they span multiple lines, catching a common class of mistake. Affected tags: `@aliases`, `@concept`, `@encoding`, `@exportClass`, `@exportMethod`, `@exportPattern`, `@exportS3Method`, `@importFrom`, `@importClassesFrom`, `@importMethodsFrom`, `@include`, `@keywords`, `@method`, `@name`, `@order`, `@rdname`, `@S3method`, `@template`, and `@useDynLib` (#1642, #1688). This may break some existing usage, but it prevents a wide range of otherwise silent errors.
+* Tags that expect single-line input now warn when they span multiple lines, catching a common class of mistake. Affected tags: `@aliases`, `@concept`, `@encoding`, `@exportClass`, `@exportMethod`, `@exportPattern`, `@exportS3Method`, `@importFrom`, `@importClassesFrom`, `@importMethodsFrom`, `@include`, `@includeRmd`, `@inheritDotParams`, `@inheritParams`, `@inheritSection`, `@keywords`, `@method`, `@name`, `@order`, `@rdname`, `@S3method`, `@template`, and `@useDynLib` (#1642, #1688). This may break some existing usage, but it prevents a wide range of otherwise silent errors.
 * Reexported functions now display with `()` appended (e.g. `fun()` instead of `fun`) on the reexports page, except for infix operators like `%>%` (#1222). They also use the modern (>= 4.1.0) linking style.
 * `@description` no longer errors when the markdown text starts with a heading (#1705).
 * `@examples` no longer warns about unmatched braces inside raw strings, or inside strings within R comments, e.g. `# '{greeting}'` (#1492).
diff --git a/R/rd-describe-in.R b/R/rd-describe-in.R
index 3d6b480e..72c5a664 100644
--- a/R/rd-describe-in.R
+++ b/R/rd-describe-in.R
@@ -10,7 +10,7 @@ roxy_tag_parse.roxy_tag_describeIn <- function(x) {
     )
     NULL
   } else {
-    tag_two_part(x, "a topic name", "a description")
+    tag_two_part(x, "a topic name", "a description", multiline = TRUE)
   }
 }
 
diff --git a/R/rd-params.R b/R/rd-params.R
index b06277f1..4edb6777 100644
--- a/R/rd-params.R
+++ b/R/rd-params.R
@@ -1,6 +1,6 @@
 #' @export
 roxy_tag_parse.roxy_tag_param <- function(x) {
-  tag_two_part(x, "an argument name", "a description")
+  tag_two_part(x, "an argument name", "a description", multiline = TRUE)
 }
 
 #' @export
diff --git a/R/rd-s4.R b/R/rd-s4.R
index faeb3333..e22c3d2f 100644
--- a/R/rd-s4.R
+++ b/R/rd-s4.R
@@ -1,6 +1,6 @@
 #' @export
 roxy_tag_parse.roxy_tag_field <- function(x) {
-  tag_two_part(x, "a field name", "a description")
+  tag_two_part(x, "a field name", "a description", multiline = TRUE)
 }
 #' @export
 roxy_tag_rd.roxy_tag_field <- function(x, base_path, env) {
@@ -14,7 +14,7 @@ format.rd_section_field <- function(x, ...) {
 
 #' @export
 roxy_tag_parse.roxy_tag_slot <- function(x) {
-  tag_two_part(x, "a slot name", "a description")
+  tag_two_part(x, "a slot name", "a description", multiline = TRUE)
 }
 #' @export
 roxy_tag_rd.roxy_tag_slot <- function(x, base_path, env) {
diff --git a/R/rd-s7.R b/R/rd-s7.R
index a092c397..d9d8864e 100644
--- a/R/rd-s7.R
+++ b/R/rd-s7.R
@@ -1,6 +1,6 @@
 #' @export
 roxy_tag_parse.roxy_tag_prop <- function(x) {
-  x <- tag_two_part(x, "a property name", "a description")
+  x <- tag_two_part(x, "a property name", "a description", multiline = TRUE)
   if (is.null(x)) {
     return()
   }
diff --git a/R/rd-template.R b/R/rd-template.R
index 1fbf1fc3..9bca3cfe 100644
--- a/R/rd-template.R
+++ b/R/rd-template.R
@@ -5,7 +5,7 @@ roxy_tag_parse.roxy_tag_template <- function(x) {
 
 #' @export
 roxy_tag_parse.roxy_tag_templateVar <- function(x) {
-  tag_two_part(x, "a variable name", "a value")
+  tag_two_part(x, "a variable name", "a value", multiline = TRUE)
 }
 
 process_templates <- function(block, base_path) {
diff --git a/R/tag-parser.R b/R/tag-parser.R
index 60bf3fbc..0ee91f71 100644
--- a/R/tag-parser.R
+++ b/R/tag-parser.R
@@ -119,7 +119,14 @@ tag_name <- function(x) {
 #' @param required Is the second part required (TRUE) or can it be blank
 #'   (FALSE)?
 #' @param markdown Should the second part be parsed as markdown?
-tag_two_part <- function(x, first, second, required = TRUE, markdown = TRUE) {
+tag_two_part <- function(
+  x,
+  first,
+  second,
+  required = TRUE,
+  markdown = TRUE,
+  multiline = FALSE
+) {
   if (trimws(x$raw) == "") {
     if (!required) {
       warn_roxy_tag(x, "requires {first}")
@@ -127,6 +134,8 @@ tag_two_part <- function(x, first, second, required = TRUE, markdown = TRUE) {
       warn_roxy_tag(x, "requires two parts: {first} and {second}")
     }
     NULL
+  } else if (!multiline && warn_if_multiline(x, trimws(x$raw))) {
+    NULL
   } else if (!rdComplete(x$raw, is_code = FALSE)) {
     warn_roxy_tag(x, "has mismatched braces or quotes")
     NULL
diff --git a/man/tag_parsers.Rd b/man/tag_parsers.Rd
index cf534ede..820a25be 100644
--- a/man/tag_parsers.Rd
+++ b/man/tag_parsers.Rd
@@ -22,7 +22,14 @@ tag_inherit(x)
 
 tag_name(x)
 
-tag_two_part(x, first, second, required = TRUE, markdown = TRUE)
+tag_two_part(
+  x,
+  first,
+  second,
+  required = TRUE,
+  markdown = TRUE,
+  multiline = FALSE
+)
 
 tag_name_description(x)
 
diff --git a/tests/testthat/_snaps/tag-parser.md b/tests/testthat/_snaps/tag-parser.md
index 4f89e298..b5d52f68 100644
--- a/tests/testthat/_snaps/tag-parser.md
+++ b/tests/testthat/_snaps/tag-parser.md
@@ -182,6 +182,17 @@
       x test.R:1: @test must be only 1 line long, not 3.
       i The first line is "a"
 
+# tag_two_part() warns on multi-line content by default
+
+    Code
+      tag <- roxy_test_tag("foo bar\nbaz")
+      expect_parse_failure(tag_two_part(tag, "a name", "a value"))
+    Output
+      <message/rlang_message>
+      Message:
+      x test.R:1: @test must be only 1 line long, not 2.
+      i The first line is "foo bar"
+
 # tag_value() warns on multi-line content
 
     Code
diff --git a/tests/testthat/test-tag-parser.R b/tests/testthat/test-tag-parser.R
index fcb4d5ad..4c06ffcc 100644
--- a/tests/testthat/test-tag-parser.R
+++ b/tests/testthat/test-tag-parser.R
@@ -87,6 +87,17 @@ test_that("tag_words() warns on multi-line content", {
   })
 })
 
+test_that("tag_two_part() warns on multi-line content by default", {
+  expect_snapshot({
+    tag <- roxy_test_tag("foo bar\nbaz")
+    expect_parse_failure(tag_two_part(tag, "a name", "a value"))
+  })
+
+  tag <- roxy_test_tag("foo bar\nbaz")
+  out <- tag_two_part(tag, "a name", "a value", multiline = TRUE)
+  expect_equal(out$val, list(name = "foo", description = "bar\nbaz"))
+})
+
 test_that("tag_value() warns on multi-line content", {
   expect_snapshot({
     tag <- roxy_test_tag("a\nb")